Cited by 26

The DOI matches its Crossref record; 1 of the 1 references it cites were found in a registry or an index.

Presence of Histatin-1 in Human Tears and Association with Aqueous Deficient Dry Eye Diagnosis: A Preliminary Study

Kalmodia, Sushma, Son, Kyung-No, Cao, Dingcai, Lee, Bao-Shiang, Surenkhuu, Bayasgalan, Shah, Dhara, Ali, Marwan, Balasubramaniam, Arun, Jain, Sandeep, Aakalu, Vinay Kumar·2019·Scientific Reports

Abstract

The aims of this study were to determine if histatin-1 (H1) is present in normal human tears and whether tear levels of H1 varied between normal patients and those with aqueous deficient dry eye disease (ADDE). Patient samples were obtained from 11 normal patients and 11 severe ADDE patients. Relevant patient characteristics, including age, sex, and dry eye disease (DED) diagnostic parameters were collected. Multiple qualitative and quantitative methods were used to compare the concentration of H1 between patient groups. Mixed linear modeling was used to compare H1 levels between groups, and diagnostic performance was assessed using the receiver-operator-characteristic (ROC). ADDE patients had significantly lower H1 concentrations (85.9 ± 63.7 ng/ml) than the normal group (891.6 ± 196.5 ng/ml) (p < 0.001), while controlling for age and sex. ROC analysis indicated that H1 concentration is potentially a biomarker for ADDE (area under curve = 0.96). Reclassification of patients by DED parameters including, Ocular Surface Disease Index (OSDI) (≤13, >13) and Schirmer I (without anesthesia) (<10 mm, ≥10 mm) showed significant differences in H1 level (OSDI, p = 0.004) and Schirmer I ((p = 0.010). In conclusion, this is the first preliminary report of the presence of H1 in human tears. H1 concentrations are lower in ADDE patients and H1 may have diagnostic potential in evaluation ADDE patients.

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.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1038/s41598-019-46623-9

Cites

1 of 1 references verified0 citation errors · 0 not checkable

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.

A few free checks a day · papers already verified open instantly · results are public

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?

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

Flagged first, then by citations

Research works printed but not linked: 54

  1. Stapleton, F. et al. TFOS DEWS II Epidemiology Report. The Ocular Surface 15, 334–365, https://doi.org/10.1016/j.jtos.2017.05.003 (2017). · DOI
  2. Craig, J. P. et al. TFOS DEWS II Definition and Classification Report. The Ocular Surface 15, 276–283, https://doi.org/10.1016/j.jtos.2017.05.008 (2017). · DOI
  3. Bron, A. J. et al. TFOS DEWS II pathophysiology report. The Ocular Surface 15, 438–510, https://doi.org/10.1016/j.jtos.2017.05.011 (2017). · DOI
  4. De Smet, K. & Contreras, R. Human antimicrobial peptides: defensins, cathelicidins and histatins. Biotechnol Lett 27, 1337–1347, https://doi.org/10.1007/s10529-005-0936-5 (2005). · DOI
  5. Hancock, R. E. W., Haney, E. F. & Gill, E. E. The immunology of host defence peptides: beyond antimicrobial activity. Nature Reviews Immunology, Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved, https://doi.org/10.1038/nri.2016.29, https://www.nature.com/articles/nri.2016.29#supplementary-information 16, 321 (2016). · DOI
  6. Khurshid, Z. et al. Histatin peptides: Pharmacological functions and their applications in dentistry. Saudi Pharmaceutical Journal 25, 25–31, https://doi.org/10.1016/j.jsps.2016.04.027 (2017). · DOI
  7. Imamura, Y. & Wang, P.-L. Salivary histatin 3 inhibits heat shock cognate protein 70-mediated inflammatory cytokine production through toll-like receptors in human gingival fibroblasts. Journal of Inflammation 11, 4, https://doi.org/10.1186/1476-9255-11-4 (2014). · DOI
  8. Vitorino, R. et al. The role of salivary peptides in dental caries. Biomed Chromatogr 19, 214–222, https://doi.org/10.1002/bmc.438 (2005). · DOI
  9. Campese, M., Sun, X., Bosch, J. A., Oppenheim, F. G. & Helmerhorst, E. J. Concentration and fate of histatins and acidic proline-rich proteins in the oral environment. Archives of Oral Biology 54, 345–353, https://doi.org/10.1016/j.archoralbio.2008.11.010 (2009). · DOI
  10. Melino, S., Santone, C., Di Nardo, P. & Sarkar, B. Histatins: salivary peptides with copper(II)- and zinc(II)-binding motifs: perspectives for biomedical applications. Febs j 281, 657–672, https://doi.org/10.1111/febs.12612 (2014). · DOI
  11. Jensen, J., Uhlig, T., Kvien, T. & Axell, T. Characteristics of rheumatoid arthritis patients with self‐reported sicca symptoms: evaluation of medical, salivary and oral parameters. Oral diseases 3, 254–261 (1997). · DOI
  12. Winiarczyk, M. et al. Tear film proteome in age-related macular degeneration. Graefes Arch Clin Exp Ophthalmol 256, 1127–1139, https://doi.org/10.1007/s00417-018-3984-y (2018). · DOI
  13. Giannobile, W. V. et al. Saliva as a diagnostic tool for periodontal disease: current state and future directions. Periodontol 2000 50, 52–64, https://doi.org/10.1111/j.1600-0757.2008.00288.x (2009). · DOI
  14. Huang, L. C., Jean, D., Proske, R. J., Reins, R. Y. & McDermott, A. M. Ocular Surface Expression and In Vitro Activity of Antimicrobial Peptides. Current Eye Research 32, 595–609, https://doi.org/10.1080/02713680701446653 (2007). · DOI
  15. Steele, P. S. & Rychwalski, P. Identification of antimicrobial defense peptides in human tear film by Schirmer strip extraction, Clinical Chemistry, suppl. AACC Annual Meeting; Washington, Vol. 52, Iss. S6, A20–A21 (2006).
  16. Shah, D. et al. Histatin-1 Expression in Human Lacrimal Epithelium. PLoS One 11, e0148018, https://doi.org/10.1371/journal.pone.0148018 (2016). · DOI
  17. Ubels, J. L. et al. Gene expression in human accessory lacrimal glands of Wolfring. Investigative ophthalmology & visual science 53, 6738–6747, https://doi.org/10.1167/iovs.12-10750 (2012). · DOI
  18. van Dijk, I. A. et al. Human salivary peptide histatin-1 stimulates epithelial and endothelial cell adhesion and barrier function. The FASEB Journal 31, 3922–3933 (2017). · DOI
  19. Tibrewal, S. et al. Tear fluid extracellular DNA: diagnostic and therapeutic implications in dry eye disease. Investigative ophthalmology & visual science 54, 8051–8061, https://doi.org/10.1167/iovs.13-12844 (2013). · DOI
  20. Schiffman, R. M., Christianson, M. D., Jacobsen, G., Hirsch, J. D. & Reis, B. L. Reliability and validity of the Ocular Surface Disease Index. Arch Ophthalmol 118, 615–621 (2000). · DOI
  21. Ali, M. et al. Evaluation of Accessory Lacrimal Gland in Muller’s Muscle Conjunctival Resection Specimens for Precursor Cell Markers and Biological Markers of Dry Eye Disease. Current Eye Research 42, 491–497, https://doi.org/10.1080/02713683.2016.1214966 (2017). · DOI
  22. Pult, H. & Riede-Pult, B. Comparison of subjective grading and objective assessment in meibography. Contact lens & anterior eye: the journal of the British Contact Lens Association 36, 22–27, https://doi.org/10.1016/j.clae.2012.10.074 (2013). · DOI
  23. Yeotikar, N. S. et al. Functional and Morphologic Changes of Meibomian Glands in an Asymptomatic Adult Population. Investigative ophthalmology & visual science 57, 3996–4007, https://doi.org/10.1167/iovs.15-18467 (2016). · DOI
  24. Green-Church, K. B., Nichols, K. K., Kleinholz, N. M., Zhang, L. & Nichols, J. J. Investigation of the human tear film proteome using multiple proteomic approaches. Molecular Vision 14, 456–470 (2008).
  25. Zhou, L. et al. In-depth analysis of the human tear proteome. J Proteomics 75, 3877–3885, https://doi.org/10.1016/j.jprot.2012.04.053 (2012). · DOI · Paper page
  26. Karnati, R., Laurie, D. E. & Laurie, G. W. Lacritin and the tear proteome as natural replacement therapy for dry eye. Exp Eye Res 117, 39–52, https://doi.org/10.1016/j.exer.2013.05.020 (2013). · DOI
  27. Galor, A. et al. Dry eye symptoms align more closely to non-ocular conditions than to tear film parameters. Br J Ophthalmol 99, 1126–1129, https://doi.org/10.1136/bjophthalmol-2014-306481 (2015). · DOI
  28. Shah, D., Ali, M., Shukla, D., Jain, S. & Aakalu, V. K. Effects of histatin-1 peptide on human corneal epithelial cells. PLoS One 12, e0178030, https://doi.org/10.1371/journal.pone.0178030 (2017). · DOI
  29. Torres, P., Castro, M., Reyes, M. & Torres, V. A. Histatins, wound healing, and cell migration. Oral Dis. https://doi.org/10.1111/odi.12816 (2017). · DOI
  30. Oydanich, M. et al. In Vivo Efficacy of Histatin-1 in a Rabbit Animal Model. Current Eye Research, 1–6, https://doi.org/10.1080/02713683.2018.1490772 (2018). · DOI
  31. Narayanan, S., Miller, W. L. & McDermott, A. M. Expression of human β-defensins in conjunctival epithelium: relevance to dry eye disease. Investigative ophthalmology & visual science 44, 3795–3801 (2003). · DOI
  32. Schnetler, R., Gillan, W. & Koorsen, G. Immunological and antimicrobial molecules in human tears: a review and preliminary report. African Vision and Eye Health 71, 123–132 (2012). · DOI
  33. McNamara, N. A. et al. Reduced Levels of Tear Lacritin Are Associated With Corneal Neuropathy in Patients With the Ocular Component of Sjogren’s Syndrome. Investigative ophthalmology & visual science 57, 5237–5243, https://doi.org/10.1167/iovs.16-19309 (2016). · DOI
  34. Badamchian, M. et al. Identification and quantification of thymosin β4 in human saliva and tears. Annals of the New York Academy of Sciences 1112, 458–465 (2007). · DOI
  35. Soria, J. et al. Tear proteome and protein network analyses reveal a novel pentamarker panel for tear film characterization in dry eye and meibomian gland dysfunction. Journal of Proteomics 78, 94–112, https://doi.org/10.1016/j.jprot.2012.11.017 (2013). · DOI
  36. Masoudi, S., Zhong, L., Raftery, M. J., Stapleton, F. J. & Willcox, M. D. Method development for quantification of five tear proteins using selected reaction monitoring (SRM) mass spectrometry. Investigative ophthalmology & visual science 55, 767–775 (2014). · DOI
  37. Dammeier, S. et al. Combined Targeted Analysis of Metabolites and Proteins in Tear Fluid With Regard to Clinical Applications. Translational vision science & technology 7, 22–22 (2018). · DOI
  38. Jung, J. H. et al. Proteomic analysis of human lacrimal and tear fluid in dry eye disease. Scientific Reports 7, 13363 (2017). · DOI
  39. Wong, T. T. et al. Proteomic profiling of inflammatory signaling molecules in the tears of patients on chronic glaucoma medication. Investigative ophthalmology & visual science 52, 7385–7391 (2011). · DOI
  40. Glasson, M., Stapleton, F. & Willcox, M. Lipid, lipase and lipocalin differences between tolerant and intolerant contact lens wearers. Current eye research 25, 227–235 (2002). · DOI
  41. Caffery, B. et al. Tear lipocalin and lysozyme in Sjögren and non-Sjogren dry eye. Optometry and Vision Science 85, 661–667 (2008). · DOI
  42. Grus, F. H., Sabuncuo, P. & Augustin, A. J. Analysis of tear protein patterns of dry‐eye patients using fluorescent staining dyes and two‐dimensional quantification algorithms. Electrophoresis 22, 1845–1850 (2001). · DOI
  43. Bron, A. J. et al. Methodologies to diagnose and monitor dry eye disease: report of the Diagnostic Methodology Subcommittee of the International Dry Eye WorkShop (2007). Ocular Surface 5, 108–152 (2007). · DOI
  44. Lemp, M. A. Report of the National Eye Institute/Industry workshop on Clinical Trials in Dry Eyes. The CLAO journal: official publication of the Contact Lens Association of Ophthalmologists, Inc 21, 221–232 (1995).
  45. Bron, A. J. Diagnosis of Dry Eye. Survey of Ophthalmology 45, S221–S226, https://doi.org/10.1016/S0039-6257(00)00201-0 (2001). · DOI
  46. Wolffsohn, J. S. et al. TFOS DEWS II Diagnostic Methodology report. The Ocular Surface 15, 539–574, https://doi.org/10.1016/j.jtos.2017.05.001 (2017). · DOI
  47. Ogawa, Y. et al. International Chronic Ocular Graft-vs-Host-Disease (GVHD) Consensus Group: Proposed Diagnostic Criteria for Chronic GVHD (Part I). Scientific Reports 3, 3419, https://doi.org/10.1038/srep03419 (2013). · DOI
  48. Hamrah, P., Alipour, F., Jiang, S., Sohn, J. H. & Foulks, G. N. Optimizing evaluation of Lissamine Green parameters for ocular surface staining. Eye (London, England) 25, 1429–1434, https://doi.org/10.1038/eye.2011.184 (2011). · DOI
  49. Agha-Hosseini, F., Mirzaii-Dizgah, I. & Mirjalili, N. Relationship of unstimulated saliva cortisol level with severity of oral dryness feeling in menopausal women. Aust Dent J 56, 171–174, https://doi.org/10.1111/j.1834-7819.2011.01320.x (2011). · DOI
  50. Takehara, S., Yanagishita, M., Podyma-Inoue, K. A. & Kawaguchi, Y. Degradation of MUC7 and MUC5B in human saliva. PLoS One 8, e69059, https://doi.org/10.1371/journal.pone.0069059 (2013). · DOI
  51. Sarkar, J. et al. Corneal neurotoxicity due to topical benzalkonium chloride. Investigative ophthalmology & visual science 53, 1792–1802, https://doi.org/10.1167/iovs.11-8775 (2012). · DOI
  52. Seki, H. et al. The Anti-Inflammatory and Proresolving Mediator Resolvin E1 Protects Mice from Bacterial Pneumonia and Acute Lung Injury. The Journal of Immunology 184, 836, https://doi.org/10.4049/jimmunol.0901809 (2010). · DOI
  53. Sonawane, S. et al. Ocular surface extracellular DNA and nuclease activity imbalance: a new paradigm for inflammation in dry eye disease. Investigative ophthalmology & visual science 53, 8253–8263, https://doi.org/10.1167/iovs.12-10430 (2012). · DOI
  54. Colombo, N. H. et al. Antimicrobial peptides in saliva of children with severe early childhood caries. Archives of Oral Biology 69, 40–46, https://doi.org/10.1016/j.archoralbio.2016.05.009 (2016). · DOI

Cited by

Sorted by citations

Metadata

Authors
Kalmodia, S., Son, K.-N., Cao, D., Lee, B.-S., Surenkhuu, B., Shah, D., Ali, M., Balasubramaniam, A., Jain, S., & Aakalu, V. K.
Venue
Scientific Reports
Published
2019-07-16
Volume
9
Issue
1
ISSN
2045-2322
Cited by
26
References
1
Language
en
Funders
  • U.S. Department of Health &amp; Human Services | NIH | National Eye Institute (R01 EY023656, R01 EY024966, P30 EY001792, K08 EY024339, R01 EY029409)
  • U.S. Department of Defense (W81XWH-17-1-0122)
  • Research to Prevent Blindness
  • U.S. Department of Veterans Affairs (I01BX004080)

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