The DOI matches its Crossref record; 88 of the 88 references it cites were found in a registry or an index.
Inflammatory mast cells up-regulate angiogenesis during squamous epithelial carcinogenesis
Open accessAbstract
Expression of HPV16 early region genes in basal keratinocytes of transgenic mice elicits a multistage pathway to squamous carcinoma. We report that infiltration by mast cells and activation of the matrix metalloproteinase MMP-9/gelatinase B coincides with the angiogenic switch in premalignant lesions. Mast cells infiltrate hyperplasias, dysplasias, and invasive fronts of carcinomas, but not the core of solid tumors, where they degranulate in close apposition to capillaries and epithelial basement membranes, releasing mast-cell-specific serine proteases MCP-4 (chymase) and MCP-6 (tryptase). MCP-6 is shown to be a mitogen for dermal fibroblasts that proliferate in the reactive stroma, whereas MCP-4 can activate progelatinase B and induce hyperplastic skin to become angiogenic in an in vitro bioassay. Notably, premalignant angiogenesis is abated in a mast-cell-deficient (KITW/KITWWv) HPV16 transgenic mouse. The data indicate that neoplastic progression in this model involves exploitation of an inflammatory response to tissue abnormality. Thus, regulation of angiogenesis during squamous carcinogenesis is biphasic: In hyperplasias, dysplasias, and invading cancer fronts, inflammatory mast cells are conscripted to reorganize stromal architecture and hyperactivate angiogenesis; within the cancer core, upregulation of angiogenesis factors in tumor cells apparently renders them self-sufficient at sustaining neovascularization.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“Genetic and functional experiments indicate that neutrophils, mast cells, eosinophils and activated T lymphocytes also contribute to malignancies by releasing extracellular proteases, pro-angiogenic factors and chemokines11,23–26.”
From Inflammation and cancer (2002) · cites this paper as [24]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
A genetic model for colorectal tumorigenesis
Fearon, E. R., & Vogelstein, B. (1990) · Cell · doi:10.1016/0092-8674(90)90186-i · Cited by 12,132
Molecular Mechanisms of Stress-Responsive Changes in Collagen and Elastin Networks in Skin
Aziz, J., Shezali, H., Radzi, Z., Yahya, N. A., Abu Kassim, N. H., Czernuszka, J., & Rahman, M. T. (2016) · Skin Pharmacology and Physiology · doi:10.1159/000447017 · Cited by 7,323
Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis
Hanahan, D., & Folkman, J. (1996) · Cell · doi:10.1016/s0092-8674(00)80108-7 · Cited by 6,885
Self-citationWhat Is the Evidence That Tumors Are Angiogenesis Dependent?
Folkman, J. (1990) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/82.1.4 · Cited by 4,509
Tumors: Wounds That Do Not Heal
Flier, J. S., Underhill, L. H., & Dvorak, H. F. (1986) · New England Journal of Medicine · doi:10.1056/nejm198612253152606 · Cited by 4,391
RAG-1-deficient mice have no mature B and T lymphocytes
Mombaerts, P., Iacomini, J., Johnson, R. S., Herrup, K., Tonegawa, S., & Papaioannou, V. E. (1992) · Cell · doi:10.1016/0092-8674(92)90030-g · Cited by 2,898
Proteins: Structures and Molecular Properties
Creighton, T. E. (1986) · Medical Entomology and Zoology · Cited by 2,645
Vu, T. H., Shipley, J. M., Bergers, G., Berger, J. E., Helms, J. A., Hanahan, D., Shapiro, S. D., Senior, R. M., & Werb, Z. (1998) · Cell · doi:10.1016/s0092-8674(00)81169-1 · Cited by 1,737
Self-citationThe proto-oncogene c-kit encoding a transmembrane tyrosine kinase receptor maps to the mouse W locus
Chabot, B., Stephenson, D. A., Chapman, V. M., Besmer, P., & Bernstein, A. (1988) · Nature · doi:10.1038/335088a0 · Cited by 1,339
Decrease of mast cells in W/Wv mice and their increase by bone marrow transplantation
Kitamura, Y., Go, S.-R., & Hatanaka, K. (1978) · Blood · doi:10.1182/blood.v52.2.447.bloodjournal522447 · Cited by 830
Flagged first, then by citations
Research works printed but not linked: 3
- Caughey, G.H. 1995. Mast cell chymases and tryptases: Phylog- eny, family relations, and biogenesis. In Mast cell proteases in immunology and biology (ed. G.H. Caughey), pp. 305- 329.
- Folkman, J. and D. Hanahan. 1991. Expression of the angiogenic phenotype during development of murine and human can- cer. In Origins of human cancer: A comprehensive review (ed. J. Brugge, J. Curran, E. Harlow, and F. McCormick), pp. 803-814. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
- Westphal, E. 1891. Uber mastzellen. In Farbenanalytische Ut- ersuchuugen zur Histologie und Klinik des Blutes: gesam- melte Mitt(h)eilungen (ed. P. Ehrlich), Vol. 1, p. 17. Hirsch- wald Press, Berlin, Germany.
Cited by
Sorted by citations
Items 401–500 of 945
Delineating Protease Functions During Cancer Development
Affara, N. I., Andreu, P., & Coussens, L. M. (2009) · Methods in molecular biology · doi:10.1007/978-1-60327-003-8_1 · Cited by 53
Self-citationIgE immunotherapy: A novel concept with promise for the treatment of cancer
Josephs, D. H., Spicer, J. F., Karagiannis, P., Gould, H. J., & Karagiannis, S. N. (2014) · mAbs · doi:10.4161/mabs.27029 · Cited by 58
Regulation of extravascular coagulation and fibrinolysis by heparin‐dependent mast cell chymase
Tchougounova, E., & Pejler, G. (2001) · The FASEB Journal · doi:10.1096/fj.01-0486fje · Cited by 53
Laubli, H. P., Müller, P., D’Amico, L., Buchi, M., Kashyap, A. S., & Zippelius, A. (2018) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-018-2136-x · Cited by 53
Extracellular vesicles from mast cells induce mesenchymal transition in airway epithelial cells
Yin, Y., Shelke, G. V., Lässer, C., Brismar, H., & Lötvall, J. O. (2020) · Respiratory Research · doi:10.1186/s12931-020-01346-8 · Cited by 53
Pourtier, A., Vercamer, C., BELLE, E. V., Mattot, V., Mouquet, F., & Vandenbunder, B. (2003) · Oncogene · doi:10.1038/sj.onc.1206215 · Cited by 53
“They also express proteases recently shown to be critical for skin tumor angiogenesis (Coussens et al., 1999).”
BackgroundAurora, A. B., Bałuk, P., Zhang, D., Sidhu, S., Dolganov, G., Basbaum, C. B., McDonald, D. M., & Killeen, N. P. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.175.10.6319 · Cited by 53
Guo, X., Zhai, L., Xue, R., Shi, J., Zeng, Q., & Gao, C. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17060834 · Cited by 52
Angiogenic Acceleration of Neu Induced Mammary Tumor Progression and Metastasis
Oshima, R. G., Lesperance, J., Munoz-Ritchie, V. G., Hebbard, L., Ranscht, B., Sharan, N., Muller, W. J., Hauser, C. A., & Cardiff, R. D. (2004) · Cancer Research · doi:10.1158/0008-5472.can-03-1944 · Cited by 51
“During skin tumor progression, inflammatory cells contribute metalloproteinase to mobilize VEGF from extracellular matrix (14).”
BackgroundFocus on mast cells in the tumor microenvironment: Current knowledge and future directions
Shi, S., Ye, L., Yu, X., Jin, K., & Wu, W. (2022) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2022.188845 · Cited by 53
Possible biological and translational significance of mast cells density in colorectal cancer.
Marech, I., Ammendola, M., Gadaleta, C., Zizzo, N., Oakley, C., Gadaleta, C. D., & Ranieri, G. (2014) · PubMed Central · doi:10.3748/wjg.v20.i27.8910 · Cited by 51
Myeloid-derived cells are key targets of tumor immunotherapy
Medina‐Echeverz, J., Aranda, F., & Berraondo, P. (2014) · OncoImmunology · doi:10.4161/onci.28398 · Cited by 53
“Mast cell progenitors also undergo differentiation when they reach their target tissue, adopting mast cell properties typically near vascular structures.(1) The ability of myeloid cells to adapt their specialized functions depending on the tissue context is well manipulated by the tumor microenvironment to polarize my…”
BackgroundMast cell phenotype, TNFα expression and degranulation status in non-small cell lung cancer
Shikotra, A., Ohri, C. M., Green, R. H., Waller, D. A., & Bradding, P. H. (2016) · Scientific Reports · doi:10.1038/srep38352 · Cited by 51
Angiogenic Self-Assembling Peptide Scaffolds for Functional Tissue Regeneration
Sarkar, B., Nguyen, P. K., Gao, W., Dondapati, A., Siddiqui, Z., & Kumar, V. (2018) · Biomacromolecules · doi:10.1021/acs.biomac.8b01137 · Cited by 51
Cell Component and Function of Tumor Microenvironment in Thyroid Cancer
Shin, E., & Koo, J. S. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232012578 · Cited by 50
“The mechanisms by which TMC play a role in tumor progression are as follows: (1) promotion of angiogenesis by heparin-like molecule, histamine, TNF-α, VEGF, platelet activating factor, IL-8, bFGF and prostaglandin that are secreted from TMC [41,42]; (2) promotion of tumor invasion and metastasis through extracellular…”
BackgroundXu, R., Murray, M. P., Jagirdar, J. S., Delgado, Y., & Melamed, J. (2002) · Archives of Pathology & Laboratory Medicine · doi:10.5858/2002-126-0562-ptotli · Cited by 50
Systemic and local levels of fetuin-A in calcific aortic valve stenosis
Kaden, J. J., Reinöhl, J., Blesch, B., Brueckmann, M., Haghi, D., Borggrefe, M. M., Schmitz, F., Klomfaß, S., Pillich, M., & Ortlepp, J. R. (2007) · International Journal of Molecular Medicine · doi:10.3892/ijmm.20.2.193 · Cited by 49
Darwiche, N., Ryscavage, A. O., Pérez‐Lorenzo, R., Wright, L., Bae, D.-S., Hennings, H., Yuspa, S. H., & Glick, A. B. (2007) · Oncogene · doi:10.1038/sj.onc.1210491 · Cited by 49
“Based on human studies and some experimental models that show a link between inflammation and tumor development (Coussens et al., 1999; Balkwill and Mantovani, 2001; Coussens and Werb, 2002; de Visser et al., 2005), it is widely believed that chronic inflammation acts to promote cancer development.”
BackgroundResultInfluentialBalachander, G. M., Talukdar, P. M., Debnath, M., Rangarajan, A., & Chatterjee, K. (2018) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.8b07609 · Cited by 49
Genomic patterns of allelic imbalance in disease free tissue adjacent to primary breast carcinomas
Ellsworth, D. L., Ellsworth, R. E., Love, B., Deyarmin, B., Lubert, S. M., Mittal, V., & Shriver, C. D. (2004) · Breast Cancer Research and Treatment · doi:10.1007/s10549-004-1424-7 · Cited by 50
“Recent studies examining the functional role of stroma in carcinogenesis reveal that stromal components play an active role in tumor development by initiating abnormal epithelial growth, recruiting cells that activate mitosis, and facilitating the transition from normal to diseased tissue [2, 3].”
BackgroundProteinase-Activated Receptor-2 (PAR2): A Tumor Suppressor in Skin Carcinogenesis
Rattenholl, A., Seeliger, S., Buddenkotte, J., Schön, M., Schön, M. P., Ständer, S., Vergnolle, N., & Steinhoff, M. S. (2007) · Journal of Investigative Dermatology · doi:10.1038/sj.jid.5700847 · Cited by 49
Leukocytes as paracrine regulators of metastasis and determinants of organ‐specific colonization
Erez, N., & Coussens, L. M. (2011) · International Journal of Cancer · doi:10.1002/ijc.26032 · Cited by 49
Self-citationIncreased mast cell density and protease content in actinic cheilitis
Rojas, I. G., Martínez, A., Pineda, Á., Spencer, L., Jiménez, M., & Rudolph, M. I. (2004) · Journal of Oral Pathology and Medicine · doi:10.1111/j.1600-0714.2004.00242.x · Cited by 47
Gounaris, E. G., Heiferman, M. J., Heiferman, J. R., Shrivastav, M., Vitello, D. J., Blatner, N. R., Knab, L. M., Phillips, J. D., Cheon, E. C., Grippo, P. J., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0121402 · Cited by 47
“Increased chronic colitis predispose patients to colorectal cancer (CRC) and colitis-associated cancer (CAC) [1–5].”
BackgroundTrabectedin and Plitidepsin: Drugs from the Sea that Strike the Tumor Microenvironment
Galmarini, C. M., D’Incalci, M., & Allavena, P. (2014) · Marine Drugs · doi:10.3390/md12020719 · Cited by 47
“Another inflammatory cell type, the mast cell, is also recruited early and promotes tumor progression by releasing proteases that activate angiogenesis [13].”
BackgroundImpact of immune cells on the hallmarks of cancer: A literature review
Costa, A. C., Santos, J., da Costa, R. M. G., & Medeiros, R. (2021) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2021.103541 · Cited by 48
Sáez, A. C., Schalper, J., Nicovani, S. M., & Rudolph, M. I. (2002) · International Journal of Gynecological Cancer · doi:10.1046/j.1525-1438.2002.01082.x · Cited by 46
Early Neoplastic Progression Is Complement Independent
de Visser, K. E., Korets, L. V., & Coussens, L. M. (2004) · Neoplasia · doi:10.1593/neo.04250 · Cited by 46
“eration and activating angiogenesis [37], in part by release of”
BackgroundMethodInfluentialSelf-citationChymase-positive mast cells in small sized adenocarcinoma of the lung
Nagata, M., Shijubo, N., Walls, A. F., Ichimiya, S., Abe, S., & Sato, N. (2003) · Archiv für Pathologische Anatomie und Physiologie und für Klinische Medicin · doi:10.1007/s00428-003-0842-y · Cited by 46
Neuropilin-1 on hematopoietic cells as a source of vascular development
Yamada, Y., Oike, Y., Ogawa, H., Ito, Y., Fujisawa, H., Suda, T., & Takakura, N. (2003) · Blood · doi:10.1182/blood-2002-01-0119 · Cited by 46
Mast Cells in Lung Inflammation
Moiseeva, E. P., & Bradding, P. (2011) · Advances in experimental medicine and biology · doi:10.1007/978-1-4419-9533-9_13 · Cited by 45
Ammendola, M., Sacco, R., Sammarco, G., Donato, G., Zuccalà, V., Romano, R., Luposella, M., Patruno, R., Vallicelli, C., Verdecchia, G. M., et al. (2013) · Gastroenterology Research and Practice · doi:10.1155/2013/703163 · Cited by 45
“Hindawi Publishing Corporation Gastroenterology Research and Practice Volume 2013, Article ID 703163, 5 pages http://dx.doi.org/10.1155/2013/703163”
BackgroundInfluentialNakamura, T., Kuwai, T., Kim, J.-S., Fan, D., Kim, S.-J., & Fidler, I. J. (2007) · Neoplasia · doi:10.1593/neo.07742 · Cited by 45
“[37] demonstrated that mast cells that are prevalent”
BackgroundChemokine sequestration by atypical chemokine receptors
Hansell, C. A. H., Simpson, C. V., & Nibbs, R. J. B. (2006) · Biochemical Society Transactions · doi:10.1042/bst0341009 · Cited by 45
Dermal mast cells affect the development of sunlight‐induced skin tumours
Sarchio, S. N. E., Kok, L., O’Sullivan, C., Halliday, G. M., & Byrne, S. N. (2012) · Experimental Dermatology · doi:10.1111/j.1600-0625.2012.01438.x · Cited by 45
Inflammation and Its Correlates in Regenerative Wound Healing: An Alternate Perspective
Gourevitch, D., Kossenkov, A. V., Zhang, Y., Clark, L. D., Chang, C., Showe, L. C., & Heber‐Katz, E. (2014) · Advances in Wound Care · doi:10.1089/wound.2014.0528 · Cited by 46
“It is a tryptase that can regulate clot formation, fibrinogen/integrin interactions, and is pro-angiogenic.(65,66) This has also been shown to be important in wound repair.”
Melo, F. R., Martin, S. S., Sommerhoff, C. P., & Pejler, G. (2019) · Cell Death and Disease · doi:10.1038/s41419-019-1879-4 · Cited by 44
Proietti, A., Ugolini, C., Melillo, R. M., Crisman, G., Elisei, R., Santoro, M. M., Minuto, M. N., Vitti, P., Miccoli, P., & Basolo, F. (2011) · Thyroid · doi:10.1089/thy.2011.0059 · Cited by 44
Gene expression profile in flow-associated pulmonary arterial hypertension with neointimal lesions
van Albada, M. E., Bartelds, B., Wijnberg, H. M., Mohaupt, S., Dickinson, M. G., Schoemaker, R. G., Kooi, K. A., Gerbens, F., & Berger, R. M. F. (2009) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00106.2009 · Cited by 44
“The involvement of mast cells in the development of PAH has received little attention, although they may be of specific interest since mast cells are known as potent angiogenic stimulators (8, 24).”
BackgroundThe regulatory network of the chemokine CCL5 in colorectal cancer
Zhang, X., Zhang, X., Wang, Y., Fang, Y., Li, M., Liu, X., Luo, H.-Y., & Tian, Y. (2023) · Annals of Medicine · doi:10.1080/07853890.2023.2205168 · Cited by 42
“It has been reported that MCs play a role in promoting angiogenesis switching during tumor growth [73,74], and MCs and their secreted cytokines play important roles in inflammation-mediated tumorigenesis by regulating proinflammatory cytokines and inducible inflammatory enzymes [75].”
BackgroundLeukocytes in glomerular injury
Holdsworth, S. R., & Tipping, P. G. (2007) · Seminars in Immunopathology · doi:10.1007/s00281-007-0097-9 · Cited by 43
The complexity of the complicity of mast cells in cancer
Nechushtan, H. (2009) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2009.12.015 · Cited by 43
Rey, E. O., Suárez‐Alén, F., Mallón, M. P., López‐López, J., & Carrión, A. B. (2014) · Acta Odontologica Scandinavica · doi:10.3109/00016357.2014.914570 · Cited by 43
Limoge, M., Safina, A. F., Beattie, A., Kapus, L., Truskinovsky, A. M., & Bakin, A. V. (2017) · Oncotarget · doi:10.18632/oncotarget.16022 · Cited by 43
Akt mediates an angiogenic switch in transformed keratinocytes
Segrelles, C. (2004) · Carcinogenesis · doi:10.1093/carcin/bgh132 · Cited by 43
“Among these factors, and besides VEGF, MMP2 and MMP9, are well-recognized inducers of tumor angiogenesis [19,20,80-82], whereas thrombospondin-1 (TSP-1) is considered an inhibitor [20-23,83].”
BackgroundCysteine cathepsins: regulators of antitumour immune response
Obermajer, N., Doljak, B., & Kos, J. (2006) · Expert Opinion on Biological Therapy · doi:10.1517/14712598.6.12.1295 · Cited by 42
“Mast cells have also been shown to promote malignant progression as their depletion diminishes premalignant angiogenesis and reduces proliferation of tumour cells and stromal fibroblasts [73].”
BackgroundMast cells impair the development of protective anti-tumor immunity
Wasiuk, A., Dalton, D. K., Schpero, W. L., Stan, R. V., Conejo-Garcia, J. R., & Noelle, R. J. (2012) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-012-1276-7 · Cited by 42
“ciated with increased microvascular density in many tumors [2, 4, 6, 7].”
Heparanase-Regulated Syndecan-1 Shedding Facilitates Herpes Simplex Virus 1 Egress
Hadigal, S. R., Koganti, R., Yadavalli, T., Agelidis, A. M., Suryawanshi, R. K., & Shukla, D. (2019) · Journal of Virology · doi:10.1128/jvi.01672-19 · Cited by 42
“In addition, matrix metalloproteinases have been implicated in angiogenesis by liberating vascular endothelial growth factor (VEGF) and insulin-like growth factor-1 (IGF-1) from the extracellular matrix (60, 61).”
BackgroundTabruyn, S. P., Sabatel, C., Nguyen, N.-Q.-N., Verhaeghe, C., Castermans, K., Malvaux, L., Griffioen, A. W., MARTIAL, J. A., & Struman, I. (2007) · Molecular Endocrinology · doi:10.1210/me.2007-0021 · Cited by 42
“Because others have shown that immune cells may contribute to angiogenesis (23), the beneficial effects of the 16K hPRL-induced immune response could be debatable.”
BackgroundPanagi, M., Mpekris, F., Voutouri, C., Hadjigeorgiou, A. G., Symeonidou, C., Porfyriou, E., Michael, C., Stylianou, A., Martin, J. D., Cabral, H., et al. (2024) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-24-0246 · Cited by 47
Wimberly, A. L., Forsyth, C. B., Khan, M. W., Pemberton, A. D., Khazaie, K., & Keshavarzian, A. (2013) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2012.01894.x · Cited by 43
“, 2011) as well as squamous epithelial layers (Coussens et al., 1999).”
Kormelink, T. G., Powe, D. G., Kuijpers, S. A., Abudukelimu, A., Fens, M. H. A. M., Pieters, E. H. E., der Ven, W. W. K.-V., Habashy, H. O., Ellis, I. O., Blokhuis, B. R. J., et al. (2014) · Oncotarget · doi:10.18632/oncotarget.1868 · Cited by 42
“Mast cells entering the tumor microenvironment at an early stage appear to promote angiogenesis which is crucial for tumor growth [15, 42-44].”
BackgroundSDF-1 Induces IL-8 Production and Transendothelial Migration of Human Cord Blood-Derived Mast Cells
Lin, T., Issekutz, T. B., & Marshall, J. S. (2001) · International Archives of Allergy and Immunology · doi:10.1159/000053693 · Cited by 40
“In mouse studies mast cell proteases have been demonstrated to have a critical role in the angiogenesis associated with a tumour model [”
BackgroundKhalaf, W. F., Yang, F., Shi, C., White, H. A., Bessler, W., Ingram, D. A., & Clapp, D. W. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.178.4.2527 · Cited by 40
The Immune Cells in the Development of Oral Squamous Cell Carcinoma
Caponio, V. C. A., Zhurakivska, K., Muzio, L. L., Troiano, G., & Cirillo, N. (2023) · Cancers · doi:10.3390/cancers15153779 · Cited by 39
Dannenfelser, R., Nome, M., Tahiri, A., Ursini‐Siegel, J., Vollan, H. K. M., Haakensen, V. D., Helland, Å., Naume, B., Caldas, C., Børresen‐Dale, A., et al. (2017) · Oncotarget · doi:10.18632/oncotarget.19078 · Cited by 39
The Influence of Mast Cell Mediators on Migration of SW756 Cervical Carcinoma Cells
Rudolph, M. I., Oreamuno, M. Y. V. B., Yefi, R., Luza, S., Andrews, E. M., Penissi, A. B., Garrido, P., & Rojas, I. G. (2008) · Journal of Pharmacological Sciences · doi:10.1254/jphs.fp0070736 · Cited by 39
Immune Cells as a Source and Target of Angiogenic and Lymphangiogenic Factors
Loffredo, S., Staiano, R. I., Granata, F., Genovese, A., & Marone, G. (2013) · Chemical immunology/Fortschritte der Allergielehre/Progress in allergy/Chemical immunology and allergy · doi:10.1159/000353316 · Cited by 38
Zeoli, A., Dentelli, P., Rosso, A., Togliatto, G., Trombetta, A., Damiano, L., di Celle, P. F., Pegoraro, L., Altruda, F., & Brizzi, M. F. (2008) · Blood · doi:10.1182/blood-2007-12-128215 · Cited by 38
Increased Neovascularization in Mice Lacking Tissue Inhibitor of Metalloproteinases-3
Ebrahem, Q., Qi, J. H., Sugimoto, M., Ali, M., Sears, J. E., Cutler, A., Khokha, R., Vasanji, A., & Anand‐Apte, B. (2011) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.10-5899 · Cited by 40
“More recently, there has been increasing evidence that mast cells may be critical in the “angiogenic switch” during tumor growth.(52)TNF- has been shown to play an important role in regulating mast cell function and tumor growth.”
BackgroundProteomic Analysis of Tumor Establishment and Growth in the B16-F10 Mouse Melanoma Model
Culp, W. D., Neal, R. E., Massey, R., Egevad, L., Pisa, P., & Garland, D. L. (2006) · Journal of Proteome Research · doi:10.1021/pr060059q · Cited by 38
Ammendola, M., Zuccalà, V., Patruno, R., Russo, E., Luposella, M., Amorosi, A., Vescio, G., Sammarco, G., Montemurro, S., Sarro, G. D., et al. (2012) · Updates in Surgery · doi:10.1007/s13304-012-0183-y · Cited by 37
The dual role of mast cells in tumor fate
Ribatti, D., Tamma, R., & Crivellato, E. (2018) · Cancer Letters · doi:10.1016/j.canlet.2018.07.005 · Cited by 39
Maurer, M., Taube, C., Schröder, N. W. J., Ebmeyer, J., Siebenhaar, F., Geldmacher, A., Schubert, N., & Roers, A. (2019) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2019.07.017 · Cited by 36
Density and migration of mast cells in lip squamous cell carcinoma and actinic cheilitis.
Costa, N. L., Oton‐Leite, A. F., Cheim, A. P., Alencar, R. D. C. G., Oton, G. J. B., Silva, T. A., & Batista, A. C. (2009) · PubMed · doi:10.14670/hh-24.457 · Cited by 35
“contribute to immunoregulation, matrix degradation, elastose change and angiogenesis (Tanooka et al., 1982; Flynn et al., 1991; Metcalfe et al., 1997; Coussens et al., 1999; Hart et al., 2000, 2002; Ranieri et al., 2002; Grimbaldeston et al., 2006).”
BackgroundInfluentialBałuk, P., Raymond, W. W., Ator, E., Coussens, L. M., McDonald, D. M., & Caughey, G. H. (2004) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00404.2003 · Cited by 36
“Several studies report that tumors grow more slowly in MMP-9-deficient mice (4, 8).”
BackgroundSelf-citationHeger, K., Seidler, B., Vahl, J. C., Schwartz, C., Kober, M., Klein, S., Voehringer, D., Saur, D., & Schmidt‐Supprian, M. (2013) · European Journal of Immunology · doi:10.1002/eji.201343731 · Cited by 37
Targeting mast cells: Uncovering prolific therapeutic role in myriad diseases
Singh, J., Shah, R., & Singh, D. (2016) · International Immunopharmacology · doi:10.1016/j.intimp.2016.09.019 · Cited by 37
Angiopoietin/Tie2 signaling, tumor angiogenesis and inflammatory diseases
Kobayashi, H. (2005) · Frontiers in bioscience · doi:10.2741/1561 · Cited by 35
“These cells produce an environment and promote tumor angiogenesis and tumor development by supplying proangiogenic growth factors, cytokines and proteases (15) (16) (62) (92).”
BackgroundNagarajan, P., Chin, S. S., Wang, D., Liu, S., Sinha, S., & Garrett‐Sinha, L. A. (2010) · Journal of Cell Science · doi:10.1242/jcs.062240 · Cited by 38
“Key words: Mmp, Chemokine, Differentiation, Keratinocyte, Transgenic, EGF ligand Jo ur na l o f C el l S ci en ce proliferation and migration (Cataisson et al., 2009; Coppe et al., 2008; Coussens et al., 1999; Takahashi et al., 2010).”
Fakhrjou, A., Niroumand-Oscoei, S. M., Somi, M. H., Ghojazadeh, M., Naghashi, S., & Samankan, S. (2013) · Journal of Gastrointestinal Cancer · doi:10.1007/s12029-013-9550-2 · Cited by 35
“[20] about the inflammatory role of mast cells in the up-regulation of angiogenesis during squamous epithelial carcinogenesis, it was concluded that mechanisms like release of pro-angiogenic proteases are responsible for switching inflammation to angiogenesis in mast cells.”
BackgroundRamakrishnan, G., Sundaram, J., Kamaraj, S., Anandakumar, P., & Devaki, T. (2008) · Investigational New Drugs · doi:10.1007/s10637-008-9163-y · Cited by 34
“Mast cells can secrete several proangiogenic factors, which can jump-start tumor angiogenesis switch [21].”
Siebenhaar, F., Metz, M., & Maurer, M. (2014) · Experimental Dermatology · doi:10.1111/exd.12328 · Cited by 34
Hensler, S., & Mueller, M. M. (2013) · The Cancer Journal · doi:10.1097/ppo.0000000000000010 · Cited by 34
“These mice spontaneously develop epidermal hyperplasia that progress to malignant SCCS in about 20% of mice.87 In this mouse model, mast cells infiltrate hyperplastic and dysplastic lesions as well as the invasive front of tumors and contribute to the establishment of a tumor-supporting stroma and to angiogenesis by r…”
BackgroundMast Cells and Angiogenesis in Human Plasma Cell Malignancies
Ribatti, D., Tamma, R., & Vacca, A. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20030481 · Cited by 34
“Development of squamous cell carcinoma in a human papilloma virus (HPV) 16 infected transgenic mouse model of epithelia carcinogenesis provided support for the participation of mast cells in tumor growth and angiogenesis [36,37].”
BackgroundActivation of ocular surface mast cells promotes corneal neovascularization
Cho, W., Mittal, S. K., Elbasiony, E., & Chauhan, S. K. (2020) · The Ocular Surface · doi:10.1016/j.jtos.2020.09.002 · Cited by 34
“However, the majority of the studies on mast cell-mediated angiogenesis have been limited to tumor biology [15, 16].”
BackgroundMast cells and inflammation-associated colorectal carcinogenesis
Tanaka, T., & Ishikawa, H. (2012) · Seminars in Immunopathology · doi:10.1007/s00281-012-0343-7 · Cited by 34
“It has been reported that mast cells act to promote the “angiogenic switch” during tumor growth [53].”
BackgroundTumor-Infiltrating Mast Cells in Colorectal Cancer as a Poor Prognostic Factor
Wu, X., Zou, Y., He, X., Yuan, R., Chen, Y., Lan, N., Lian, L., Wang, F., Fan, X., Zeng, Y., et al. (2012) · International Journal of Surgical Pathology · doi:10.1177/1066896912448836 · Cited by 34
Hallgren, J., Lindahl, S. B., & Pejler, G. (2004) · Journal of Molecular Biology · doi:10.1016/j.jmb.2004.10.029 · Cited by 34
Filippis, D. D., Russo, A., D’Amico, A., Esposito, G., Potenza, C., Cinelli, M. P., Russo, G., & Iuvone, T. (2008) · British Journal of Pharmacology · doi:10.1038/bjp.2008.211 · Cited by 34
“Among the mediators in MCs, the chymases, a family of serine proteases exclusively expressed in connective tissue MCs, represent interesting molecules exhibiting both proinflammatory and pro-angiogenic activities (Coussens et al., 1999).”
BackgroundSund, M., Zeisberg, M., & Kalluri, R. (2005) · Gastroenterology · doi:10.1053/j.gastro.2005.06.023 · Cited by 34
Macrophage Matrix Metalloproteinase-9 Regulates Angiogenesis in Ischemic Muscle
Bendeck, M. P. (2004) · Circulation Research · doi:10.1161/01.res.0000117525.23089.1a · Cited by 34
Gaje, P. N., Ceauşu, R. A., Jitariu, A. A., Stratul, Ş., Rusu, L. C., Popovici, R. A., & Raica, M. (2016) · BioMed Research International · doi:10.1155/2016/9235080 · Cited by 33
“Moreover, in an experimental model of carcinogenesis, mast cell density has been associated with carcinoma development through the regulation of angiogenesis during the premalignant and malignant stages of squamous epithelial carcinogenesis [75, 76].”
Extracellular DNA Traps: Origin, Function and Implications for Anti-Cancer Therapies
Mamtimin, M., Pinarci, A., Han, C., Braun, A., Anders, H., Gudermann, T. W., & Mammadova‐Bach, E. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.869706 · Cited by 35
Eichten, A., Hyun, W. C., & Coussens, L. M. (2007) · Cancer Research · doi:10.1158/0008-5472.can-06-4676 · Cited by 33
“1A), although tumor vasculature possessed angiogenic characteristics (16).”
BackgroundSelf-citationMast cells can contribute to axon–glial dissociation and fibrosis in peripheral nerve
Monk, K. R., Wu, J.-Q., Williams, J. P., Finney, B. A., Fitzgerald, M. E., Filippi, M., & Ratner, N. (2007) · Neuron Glia Biology · doi:10.1017/s1740925x08000021 · Cited by 33
“A pivotal link between inflammation and carcinogenesis is being unraveled (Coussens et al., 1999; Balkwill and Coussens, 2004; de Visser et al., 2005), and the classical view of mast cells as effectors in allergy and IgE-mediated immune response is becoming outmoded as essential, non-immunological roles for mast cells…”
BackgroundThrombospondin-1 repression is mediated via distinct mechanisms in fibroblasts and epithelial cells
Watnick, R. S., Rodriguez, R. K., Wang, S., Blois, A. L., Rangarajan, A., Ince, T. A., & Weinberg, R. A. (2014) · Oncogene · doi:10.1038/onc.2014.228 · Cited by 33
Role of hematopoietic lineage cells as accessory components in blood vessel formation
Takakura, N. (2006) · Cancer Science · doi:10.1111/j.1349-7006.2006.00223.x · Cited by 33
Host manipulation by cancer cells: Expectations, facts, and therapeutic implications
Tissot, T., Arnal, A., Jacqueline, C. M., Poulin, R., Léfèvre, T., Mery, F., Renaud, F., Roche, B., Massol, F., Salzet, M., et al. (2016) · BioEssays · doi:10.1002/bies.201500163 · Cited by 37
“Additionally, innate immune cells promote angiogenesis by the production of growth factors and chemokines [38, 40], and in many cancers, the release of CXC chemokines recruits endothelial cells into angiogenesis [41, 42].”
BackgroundMast Cells and Skin and Breast Cancers: A Complicated and Microenvironment-Dependent Role
Hanes, M. R., Giacomantonio, C. A., & Marshall, J. S. (2021) · Cells · doi:10.3390/cells10050986 · Cited by 33
“Cg-KitW-sh/W-sh (Wsh) and WBB6F1/J-KitW/KitW-v/J [19,33].”
BackgroundResultLIN, Y.-W., Lai, H.-C., Lin, C., Chiou, J. Y., Shui, H.-A., Chang, C., Yu, M. H., & Chu, T. (2006) · International Journal of Gynecological Cancer · doi:10.1111/j.1525-1438.2006.00583.x · Cited by 32
Mast cells promote melanoma colonization of lungs
Öhrvik, H., Grujić, M., Waern, I., Gustafson, A., Ernst, N., Roers, A., Hartmann, K., & Pejler, G. (2016) · Oncotarget · doi:10.18632/oncotarget.11837 · Cited by 32
“To experimentally address the role of mast cells in malignancies, investigators have assessed various mast celldeficient mouse models, mainly such in which mast celldeficiency is a result of defective c-kit signaling [26-31].”
BackgroundGarton, A. J., Seibel, S., Lopresti-Morrow, L., Crew, L., Janson, N., Mandiyan, S., Trombetta, E. S., Pankratz, S., LaVallee, T. M., & Gedrich, R. (2017) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-16-0676 · Cited by 32
Thinking beyond the tumor cell: Nf1 haploinsufficiency in the tumor environment
McLaughlin, M. E., & Jacks, T. (2002) · Cancer Cell · doi:10.1016/s1535-6108(02)00078-8 · Cited by 32
Jo, J. Y., Chae, S. J., & Ryu, H. J. (2024) · Annals of Dermatology · doi:10.5021/ad.23.133 · Cited by 31
“The role of histamine in melanogenesis is still unclear, but it is thought to be related to growth-dif-ferentiation factor-15 (GDF-15), which belongs to the transforming growth factor (TGF-β ) superfamily 15 .”
BackgroundThe Hallmarks of Cancer Review
Hanahan, D., & Weinberg, R. A. (2000) · Cited by 31
Self-citationVaszar, L. T., Nishimura, T., Storey, J. D., Zhao, G., Qiu, D., Faul, J. L., Pearl, R. G., & Kao, P. N. (2004) · Physiological Genomics · doi:10.1152/physiolgenomics.00198.2003 · Cited by 31
“Chymase and tryptase are potent angiogenic signals in a variety of experimental models (4, 16).”
BackgroundIgE‐based immunotherapy of cancer: challenges and chances
Singer, J., & Jensen‐Jarolim, E. (2013) · Allergy · doi:10.1111/all.12276 · Cited by 30
“However, there is strong evidence for mast cell-related angiogenesis in tumor growth (138, 145, 146), and also, the multiple immunomodulatory effects of mast cells are intensively investigated, which will clarify the enigmatic role of mast cells in malignant disease.”
BackgroundThe Plexiform Neurofibroma Microenvironment
Yang, F., Staser, K. W., & Clapp, D. W. (2012) · Cancer Microenvironment · doi:10.1007/s12307-012-0115-x · Cited by 30
Maltby, S., Freeman, S. A., Gold, M. J., Baker, J. H. E., Minchinton, A. I., Gold, M. R., Roskelley, C. D., & McNagny, K. M. (2011) · PLoS ONE · doi:10.1371/journal.pone.0018160 · Cited by 30
Metadata
- Authors
- Coussens, L. M., Raymond, W. W., Bergers, G., Laig-Webster, M., Behrendtsen, O., Werb, Z., Caughey, G. H., & Hanahan, D.
- Affiliations
- University of California, San Francisco (US)
- Venue
- Genes & Development
- Publisher
- Cold Spring Harbor Laboratory
- Published
- 1999-06-01
- Volume
- 13
- Issue
- 11
- Pages
- 1382-1397
- ISSN
- 0890-9369 (ISSN-L)
- PMC
- PMC316772
- OpenAlex
- W2146440075
- Cited by
- 946
- References
- 87
- Citations by year
- 2026: 5 · 2025: 14 · 2024: 11 · 2023: 13 · 2022: 27 · 2021: 18 · 2020: 29 · 2019: 31 · 2018: 27 · 2017: 29 · 2016: 39 · 2015: 32 · 2014: 52 · 2013: 32 · 2012: 49
- Type
- posted content
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Genes & Development (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Pfizer
- National Institutes of Health
- National Heart, Lung, and Blood Institute (HL 24136, P01HL024136)
- National Cancer Institute (CA72006, P01CA072006)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
- Life Sciences › Immunology and Microbiology › Immunology › Mast cells and histamine
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Protease and Inhibitor Mechanisms
- Keywords
- mast cells, angiogenesis, squamous cell carcinoma, HPV16, keratinocytes, MMP-9, chymase, tryptase, precancerous lesions, dermal fibroblasts, tumor stroma, inflammation, carcinogenesis, neovascularization
- MeSH terms
- Animals, Carcinoma, Squamous Cell, Extracellular Matrix, Humans, Mast Cells, Mice, Transgenic, Neovascularization, Pathologic, Serine Endopeptidases, Up-Regulation, Inflammation Mediators, Mice, Tryptases, Chymases
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
