Skip to main content

Advertisement

SpringerLink
Log in

Study of small proline-rich proteins (SPRRs) in health and disease: a review of the literature

  • Review Article
  • Published:
Archives of Dermatological Research Aims and scope Submit manuscript

Abstract

Epithelial tissues are specialized to protect underlying tissues from environmental influences such as physical and chemical agents, infection by invasive microorganisms as well as water and heat loss. They are grouped into simple, transitional and stratified epithelia, which line the cavities and surfaces of structures throughout the body, and also form glands, separate compartments, regulate the exchange of molecules and act as sensory organs. Stratified epithelia such as the epidermis and the gingival and hard palate mucosa are in constant renewal, with cells proliferating in the lower layers, while the intermediate stratum and outermost layers undergo a tissue-specific process of differentiation to form a protective cornified barrier. This review focuses on a subclass of structural proteins, the small proline-rich proteins (SPRRs), which constitute cornified cell envelope precursors. Several studies have suggested that the SPRRs are related to increased epithelial proliferation and to malignant processes. Hence, we also review the literature for more extensive and in-depth profile of these proteins in cancer and other diseases. The understanding of SPRR functions has advanced in recent years, but many important questions about their role in pathophysiological processes remain unanswered, which stimulate new studies and approaches.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Abraham JM, Wang S, Suzuki H, Jiang HY, Rosenblum-Vos LS, Yin J, Meltzer SJ (1996) Esophagin cDNA cloning and characterization: a tissue-specific member of the small proline-rich protein family that is not expressed in esophageal tumors. Cell Growth Differentiation Mol Biol J Am Assoc Cancer Res 7(7):855–860

    CAS  Google Scholar 

  2. Alberts B, Johnson A, Lewis J (2002) Molecular biology of the cell. In: 4 edn. Garland science

  3. Arnson Y, Shoenfeld Y, Amital H (2010) Effects of tobacco smoke on immunity, inflammation and autoimmunity. J Autoimmun 34(3):J258–J265. doi:10.1016/j.jaut.2009.12.003

    Article  PubMed  CAS  Google Scholar 

  4. Backendorf C, Hohl D (1992) A common origin for cornified envelope proteins? Nat Genet 2(2):91. doi:10.1038/ng1092-91

    Article  PubMed  CAS  Google Scholar 

  5. Bracken S, Byrne G, Kelly J, Jackson J, Feighery C (2008) Altered gene expression in highly purified enterocytes from patients with active coeliac disease. BMC Genomics 9:377. doi:10.1186/1471-2164-9-377

    Article  PubMed  Google Scholar 

  6. Bragulla HH, Homberger DG (2009) Structure and functions of keratin proteins in simple, stratified, keratinized and cornified epithelia. J Anat 214(4):516–559. doi:10.1111/j.1469-7580.2009.01066.x

    Article  PubMed  CAS  Google Scholar 

  7. Burton MJ, Rajak SN, Bauer J, Weiss HA, Tolbert SB, Shoo A, Habtamu E, Manjurano A, Emerson PM, Mabey DC, Holland MJ, Bailey RL (2011) Conjunctival transcriptome in scarring trachoma. Infect Immun 79(1):499–511. doi:10.1128/IAI.00888-10

    Article  PubMed  CAS  Google Scholar 

  8. Cabral A, Sayin A, de Winter S, Fischer DF, Pavel S, Backendorf C (2001) SPRR4, a novel cornified envelope precursor: UV-dependent epidermal expression and selective incorporation into fragile envelopes. J Cell Sci 114(Pt 21):3837–3843

    PubMed  CAS  Google Scholar 

  9. Cabral A, Voskamp P, Cleton-Jansen AM, South A, Nizetic D, Backendorf C (2001) Structural organization and regulation of the small proline-rich family of cornified envelope precursors suggest a role in adaptive barrier function. J Biol Chem 276(22):19231–19237. doi:10.1074/jbc.M100336200

    Article  PubMed  CAS  Google Scholar 

  10. Candi E, Schmidt R, Melino G (2005) The cornified envelope: a model of cell death in the skin. Nat Rev Mol Cell Biol 6(4):328–340. doi:10.1038/nrm1619

    Article  PubMed  CAS  Google Scholar 

  11. Chen Z, Tong L, Li Z, Yoon KC, Qi H, Farley W, Li DQ, Pflugfelder SC (2008) Hyperosmolarity-induced cornification of human corneal epithelial cells is regulated by JNK MAPK. Invest Ophthalmol Vis Sci 49(2):539–549. doi:10.1167/iovs.07-0569

    Article  PubMed  Google Scholar 

  12. Cho DH, Jo YK, Roh SA, Na YS, Kim TW, Jang SJ, Kim YS, Kim JC (2010) Upregulation of SPRR3 promotes colorectal tumorigenesis. Mol Med 16(7–8):271–277. doi:10.2119/molmed.2009.00187

    PubMed  CAS  Google Scholar 

  13. de AST, Souza-Santos PT, de Oliveira DS, Bernardo V, Lima SC, Rapozo DC, Kruel CD, Faria PA, Ribeiro Pinto LF, Albano RM (2011) Quantitative evaluation of SPRR3 expression in esophageal squamous cell carcinoma by qPCR and its potential use as a biomarker. Exp Mol Pathol 91(2):584–589. doi:10.1016/j.yexmp.2011.06.006

  14. De Heller-Milev M, Huber M, Panizzon R, Hohl D (2000) Expression of small proline rich proteins in neoplastic and inflammatory skin diseases. Br J Dermatol 143(4):733–740

    Article  PubMed  Google Scholar 

  15. De Paiva CS, Villarreal AL, Corrales RM, Rahman HT, Chang VY, Farley WJ, Stern ME, Niederkorn JY, Li DQ, Pflugfelder SC (2007) Dry eye-induced conjunctival epithelial squamous metaplasia is modulated by interferon-gamma. Invest Ophthalmol Vis Sci 48(6):2553–2560. doi:10.1167/iovs.07-0069

    Article  PubMed  Google Scholar 

  16. Demetris AJ, Specht S, Nozaki I, Lunz JG 3rd, Stolz DB, Murase N, Wu T (2008) Small proline-rich proteins (SPRR) function as SH3 domain ligands, increase resistance to injury and are associated with epithelial-mesenchymal transition (EMT) in cholangiocytes. J Hepatol 48(2):276–288. doi:10.1016/j.jhep.2007.09.019

    Article  PubMed  CAS  Google Scholar 

  17. DeMuth JP, Weaver DA, Crawford EL, Jackson CM, Willey JC (1998) Loss of spr1 expression measurable by quantitative RT-PCR in human bronchogenic carcinoma cell lines. Am J Respir Cell Mol Biol 19(1):25–29. doi:10.1165/ajrcmb.19.1.3078

    Article  PubMed  CAS  Google Scholar 

  18. Fasano A, Catassi C (2012) Clinical practice. Celiac disease. New Engl J Med 367(25):2419–2426. doi:10.1056/NEJMcp1113994

    Article  PubMed  CAS  Google Scholar 

  19. Felsenstein J (1985) Confidence limits on phytogenies: an approach using the bootstrap. Evolution 39(4):783–791

    Article  Google Scholar 

  20. Fischer DF, Backendorf C (2007) Identification of regulatory elements by gene family footprinting and in vivo analysis. Adv Biochem Eng Biotechnol 104:37–64

    PubMed  CAS  Google Scholar 

  21. Fischer DF, Gibbs S, van De Putte P, Backendorf C (1996) Interdependent transcription control elements regulate the expression of the SPRR2A gene during keratinocyte terminal differentiation. Mol Cell Biol 16(10):5365–5374

    PubMed  CAS  Google Scholar 

  22. Fischer DF, Sark MW, Lehtola MM, Gibbs S, van de Putte P, Backendorf C (1999) Structure and evolution of the human SPRR3 gene: implications for function and regulation. Genomics 55(1):88–99. doi:10.1006/geno.1998.5622

    Article  PubMed  CAS  Google Scholar 

  23. Fuchs E (1995) Keratins and the skin. Ann Rev Cell Dev Biol 11:123–153. doi:10.1146/annurev.cb.11.110195.001011

    Article  CAS  Google Scholar 

  24. Fujimoto W, Nakanishi G, Arata J, Jetten AM (1997) Differential expression of human cornifin alpha and beta in squamous differentiating epithelial tissues and several skin lesions. J Invest Dermatol 108(2):200–204

    Article  PubMed  CAS  Google Scholar 

  25. Garmyn M, Yaar M, Boileau N, Backendorf C, Gilchrest BA (1992) Effect of aging and habitual sun exposure on the genetic response of cultured human keratinocytes to solar-simulated irradiation. J Invest Dermatol 99(6):743–748

    Article  PubMed  CAS  Google Scholar 

  26. Gibbs S, Fijneman R, Wiegant J, van Kessel AG, van De Putte P, Backendorf C (1993) Molecular characterization and evolution of the SPRR family of keratinocyte differentiation markers encoding small proline-rich proteins. Genomics 16(3):630–637. doi:10.1006/geno.1993.1240

    Article  PubMed  CAS  Google Scholar 

  27. Glotzer M (2009) The 3Ms of central spindle assembly: microtubules, motors and MAPs. Nat Rev Mol Cell Biol 10(1):9–20. doi:10.1038/nrm2609

    Article  PubMed  CAS  Google Scholar 

  28. Hanakawa Y, Amagai M, Shirakata Y, Yahata Y, Tokumaru S, Yamasaki K, Tohyama M, Sayama K, Hashimoto K (2002) Differential effects of desmoglein 1 and desmoglein 3 on desmosome formation. J Invest Dermatol 119(6):1231–1236. doi:10.1046/j.1523-1747.2002.19648.x

    Article  PubMed  CAS  Google Scholar 

  29. Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22(2):160–174

    Article  PubMed  CAS  Google Scholar 

  30. Hoffjan S, Stemmler S (2007) On the role of the epidermal differentiation complex in ichthyosis vulgaris, atopic dermatitis and psoriasis. Br J Dermatol 157(3):441–449. doi:10.1111/j.1365-2133.2007.07999.x

    Article  PubMed  CAS  Google Scholar 

  31. Hohl D, de Viragh PA, Amiguet-Barras F, Gibbs S, Backendorf C, Huber M (1995) The small proline-rich proteins constitute a multigene family of differentially regulated cornified cell envelope precursor proteins. J Invest Dermatol 104(6):902–909

    Article  PubMed  CAS  Google Scholar 

  32. Hu R, Wu R, Deng J, Lau D (1998) A small proline-rich protein, spr1: specific marker for squamous lung carcinoma. Lung Cancer 20(1):25–30

    Article  PubMed  CAS  Google Scholar 

  33. Ishida-Yamamoto A, Iizuka H, Manabe M, O’Guin WM, Hohl D, Kartasova T, Kuroki T, Roop DR, Eady RA (1995) Altered distribution of keratinization markers in epidermolytic hyperkeratosis. Arch Dermatol Res 287(8):705–711

    Article  PubMed  CAS  Google Scholar 

  34. Jarzab J, Filipowska B, Zebracka J, Kowalska M, Bozek A, Rachowska R, Gubala E, Grzanka A, Hadas E, Jarzab B (2010) Locus 1q21 Gene expression changes in atopic dermatitis skin lesions: deregulation of small proline-rich region 1A. Int Arch Allerg Immunol 151(1):28–37. doi:10.1159/000232568

    Article  CAS  Google Scholar 

  35. Jetten AM, Harvat BL (1997) Epidermal differentiation and squamous metaplasia: from stem cell to cell death. J Dermatol 24(11):711–725

    PubMed  CAS  Google Scholar 

  36. Kainu K, Kivinen K, Zucchelli M, Suomela S, Kere J, Inerot A, Baker BS, Powles AV, Fry L, Samuelsson L, Saarialho-Kere U (2009) Association of psoriasis to PGLYRP and SPRR genes at PSORS4 locus on 1q shows heterogeneity between Finnish Swedish and Irish families. Exp Dermatol 18(2):109–115. doi:10.1111/j.1600-0625.2008.00769.x

    Article  PubMed  CAS  Google Scholar 

  37. Kalinin A, Marekov LN, Steinert PM (2001) Assembly of the epidermal cornified cell envelope. J Cell Sci 114(Pt 17):3069–3070

    PubMed  CAS  Google Scholar 

  38. Kartasova T, Darwiche N, Kohno Y, Koizumi H, Osada S, Huh N, Lichti U, Steinert PM, Kuroki T (1996) Sequence and expression patterns of mouse SPR1: correlation of expression with epithelial function. J Invest Dermatol 106(2):294–304

    Article  PubMed  CAS  Google Scholar 

  39. Kartasova T, van de Putte P (1988) Isolation, characterization, and UV-stimulated expression of two families of genes encoding polypeptides of related structure in human epidermal keratinocytes. Mol Cell Biol 8(5):2195–2203

    PubMed  CAS  Google Scholar 

  40. Kartasova T, van Muijen GN, van Pelt-Heerschap H, van de Putte P (1988) Novel protein in human epidermal keratinocytes: regulation of expression during differentiation. Mol Cell Biol 8(5):2204–2210

    PubMed  CAS  Google Scholar 

  41. Kim JC, Yu JH, Cho YK, Jung CS, Ahn SH, Gong G, Kim YS, Cho DH (2012) Expression of SPRR3 is associated with tumor cell proliferation in less advanced stages of breast cancer. Breast Cancer Res Treat 133(3):909–916. doi:10.1007/s10549-011-1868-5

    Article  PubMed  CAS  Google Scholar 

  42. Kimchi ET, Posner MC, Park JO, Darga TE, Kocherginsky M, Karrison T, Hart J, Smith KD, Mezhir JJ, Weichselbaum RR, Khodarev NN (2005) Progression of Barrett’s metaplasia to adenocarcinoma is associated with the suppression of the transcriptional programs of epidermal differentiation. Cancer Res 65(8):3146–3154. doi:10.1158/0008-5472.CAN-04-2490

    PubMed  CAS  Google Scholar 

  43. Koizumi H, Kartasova T, Tanaka H, Ohkawara A, Kuroki T (1996) Differentiation-associated localization of small proline-rich protein in normal and diseased human skin. Br J Dermatol 134(4):686–692

    Article  PubMed  CAS  Google Scholar 

  44. Lau D, Xue L, Hu R, Liaw T, Wu R, Reddy S (2000) Expression and regulation of a molecular marker, SPR1, in multistep bronchial carcinogenesis. Am J Respir Cell Mol Biol 22(1):92–96. doi:10.1165/ajrcmb.22.1.3637

    Article  PubMed  CAS  Google Scholar 

  45. Lee CH, Marekov LN, Kim S, Brahim JS, Park MH, Steinert PM (2000) Small proline-rich protein 1 is the major component of the cell envelope of normal human oral keratinocytes. FEBS Lett 477(3):268–272

    Article  PubMed  CAS  Google Scholar 

  46. Lee J, Taneja V, Vassallo R (2012) Cigarette smoking and inflammation: cellular and molecular mechanisms. J Dent Res 91(2):142–149. doi:10.1177/0022034511421200

    Article  PubMed  CAS  Google Scholar 

  47. Li S, Nikulina K, DeVoss J, Wu AJ, Strauss EC, Anderson MS, McNamara NA (2008) Small proline-rich protein 1B (SPRR1B) is a biomarker for squamous metaplasia in dry eye disease. Invest Ophthalmol Vis Sci 49(1):34–41. doi:10.1167/iovs.07-0685

    Article  PubMed  Google Scholar 

  48. Lohman FP, Medema JK, Gibbs S, Ponec M, van de Putte P, Backendorf C (1997) Expression of the SPRR cornification genes is differentially affected by carcinogenic transformation. Exp Cell Res 231(1):141–148. doi:10.1006/excr1996.3458

    Article  PubMed  CAS  Google Scholar 

  49. Lubrano E, Ciacci C, Ames PR, Mazzacca G, Oriente P, Scarpa R (1996) The arthritis of coeliac disease: prevalence and pattern in 200 adult patients. Br J Rheumatol 35(12):1314–1318

    Article  PubMed  CAS  Google Scholar 

  50. Luo A, Kong J, Hu G, Liew CC, Xiong M, Wang X, Ji J, Wang T, Zhi H, Wu M, Liu Z (2004) Discovery of Ca2+ -relevant and differentiation-associated genes downregulated in esophageal squamous cell carcinoma using cDNA microarray. Oncogene 23(6):1291–1299. doi:10.1038/sj.onc.1207218

    Article  PubMed  CAS  Google Scholar 

  51. Marshall D, Hardman MJ, Nield KM, Byrne C (2001) Differentially expressed late constituents of the epidermal cornified envelope. Proc Natl Acad Sci USA 98(23):13031–13036. doi:10.1073/pnas.231489198

    Article  PubMed  CAS  Google Scholar 

  52. Martin N, Patel S, Segre JA (2004) Long-range comparison of human and mouse Sprr loci to identify conserved noncoding sequences involved in coordinate regulation. Genome Res 14(12):2430–2438. doi:10.1101/gr.2709404

    Article  PubMed  CAS  Google Scholar 

  53. Martinet N, Beninati S, Nigra TP, Folk JE (1990) N1N8-bis(gamma-glutamyl)spermidine cross-linking in epidermal-cell envelopes. Comparison of cross-link levels in normal and psoriatic cell envelopes. Biochem J 271(2):305–308

    PubMed  CAS  Google Scholar 

  54. Maru DM, Singh RR, Hannah C, Albarracin CT, Li YX, Abraham R, Romans AM, Yao H, Luthra MG, Anandasabapathy S, Swisher SG, Hofstetter WL, Rashid A, Luthra R (2009) MicroRNA-196a is a potential marker of progression during Barrett’s metaplasia-dysplasia-invasive adenocarcinoma sequence in esophagus. Am J Pathol 174(5):1940–1948. doi:10.2353/ajpath.2009.080718

    Article  PubMed  CAS  Google Scholar 

  55. McLean WH, Irvine AD (2007) Disorders of keratinisation: from rare to common genetic diseases of skin and other epithelial tissues. Ulster Med J 76(2):72–82

    PubMed  Google Scholar 

  56. Mischke D, Korge BP, Marenholz I, Volz A, Ziegler A (1996) Genes encoding structural proteins of epidermal cornification and S100 calcium-binding proteins form a gene complex (“epidermal differentiation complex”) on human chromosome 1q21. J Invest Dermatol 106(5):989–992

    Article  PubMed  CAS  Google Scholar 

  57. Mizuguchi Y, Specht S, Lunz JG 3rd, Isse K, Corbitt N, Takizawa T, Demetris AJ (2012) SPRR2A enhances p53 deacetylation through HDAC1 and down regulates p21 promoter activity. BMC Mol Biol 13:20. doi:10.1186/1471-2199-13-20

    Article  PubMed  CAS  Google Scholar 

  58. Okuyama R, Tagami H, Aiba S (2008) Notch signaling: its role in epidermal homeostasis and in the pathogenesis of skin diseases. J Dermatol Sci 49(3):187–194. doi:10.1016/j.jdermsci.2007.05.017

    Article  PubMed  Google Scholar 

  59. Pasini FS, Maistro S, Snitcovsky I, Barbeta LP, Rotea Mangone FR, Lehn CN, Walder F, Carvalho MB, Brentani MM, Federico MH (2012) Four-gene expression model predictive of lymph node metastases in oral squamous cell carcinoma. Acta Oncol 51(1):77–85. doi:10.3109/0284186X.2011.620619

    Article  PubMed  CAS  Google Scholar 

  60. Presland RB, Dale BA (2000) Epithelial structural proteins of the skin and oral cavity: function in health and disease. Crit Rev Oral Biol Med Off Publ Am Assoc Oral Biol 11(4):383–408

    Article  CAS  Google Scholar 

  61. Presland RB, Jurevic RJ (2002) Making sense of the epithelial barrier: what molecular biology and genetics tell us about the functions of oral mucosal and epidermal tissues. J Dent Educ 66(4):564–574

    PubMed  Google Scholar 

  62. Proksch E, Brandner JM, Jensen JM (2008) The skin: an indispensable barrier. Exp Dermatol 17(12):1063–1072

    Article  PubMed  Google Scholar 

  63. Reddy SP, Vuong H, Adiseshaiah P (2003) Interplay between proximal and distal promoter elements is required for squamous differentiation marker induction in the bronchial epithelium: role for ESE-1, Sp1, and AP-1 proteins. J Biol Chem 278(24):21378–21387. doi:10.1074/jbc.M212258200

    Article  PubMed  CAS  Google Scholar 

  64. Rinnerthaler M, Duschl J, Steinbacher P, Salzmann M, Bischof J, Schuller M, Wimmer H, Peer T, Bauer JW, Richter K (2013) Age-related changes in the composition of the cornified envelope in human skin. Exp Dermatol 22(5):329–335. doi:10.1111/exd.12135

    Article  PubMed  CAS  Google Scholar 

  65. Robinson PA, Marley JJ, High AS, Hume WJ (1994) Differential expression of protease inhibitor and small proline-rich protein genes between normal human oral tissue and odontogenic keratocysts. Arch Oral Biol 39(3):251–259

    Article  PubMed  CAS  Google Scholar 

  66. Schafer M, Werner S The cornified envelope: a first line of defense against reactive oxygen species. J Invest Dermatol 131 (7):1409–1411. doi:10.1038/jid.2011.119

  67. Segre JA (2006) Epidermal barrier formation and recovery in skin disorders. J Clin Investig 116(5):1150–1158. doi:10.1172/JCI28521

    Article  PubMed  CAS  Google Scholar 

  68. Silveira NJ, Varuzza L, Machado-Lima A, Lauretto MS, Pinheiro DG, Rodrigues RV, Severino P, Nobrega FG, Silva WA, Jr, de BPCA, Tajara EH (2008) Searching for molecular markers in head and neck squamous cell carcinomas (HNSCC) by statistical and bioinformatic analysis of larynx-derived SAGE libraries. BMC Med Genomics 1:56. doi:10.1186/1755-8794-1-56

  69. Song HJ, Poy G, Darwiche N, Lichti U, Kuroki T, Steinert PM, Kartasova T (1999) Mouse Sprr2 genes: a clustered family of genes showing differential expression in epithelial tissues. Genomics 55(1):28–42. doi:10.1006/geno1998.5607

    Article  PubMed  CAS  Google Scholar 

  70. Stamnaes J, Dorum S, Fleckenstein B, Aeschlimann D, Sollid LM (2010) Gluten T cell epitope targeting by TG3 and TG6; implications for dermatitis herpetiformis and gluten ataxia. Amino Acids 39(5):1183–1191. doi:10.1007/s00726-010-0554-y

    Article  PubMed  CAS  Google Scholar 

  71. Steinert PM, Kartasova T, Marekov LN (1998) Biochemical evidence that small proline-rich proteins and trichohyalin function in epithelia by modulation of the biomechanical properties of their cornified cell envelopes. J Biol Chem 273(19):11758–11769

    Article  PubMed  CAS  Google Scholar 

  72. Steinert PM, Marekov LN (1995) The proteins elafin, filaggrin, keratin intermediate filaments, loricrin, and small proline-rich proteins 1 and 2 are isodipeptide cross-linked components of the human epidermal cornified cell envelope. J Biol Chem 270(30):17702–17711

    Article  PubMed  CAS  Google Scholar 

  73. Steinert PM, Steven AC, Roop DR (1985) The molecular biology of intermediate filaments. Cell 42(2):411–420

    Article  PubMed  CAS  Google Scholar 

  74. Steinert PM, Wantz ML, Idler WW (1982) O-phosphoserine content of intermediate filament subunits. Biochemistry 21(1):177–183

    Article  PubMed  CAS  Google Scholar 

  75. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739. doi:10.1093/molbev/msr121

    Article  PubMed  CAS  Google Scholar 

  76. Tesfaigzi J, Carlson DM (1996) Cell cycle-specific expression of G(0)SPR1 in Chinese hamster ovary cells. Exp Cell Res 228(2):277–282. doi:10.1006/excr1996.0327

    Article  PubMed  CAS  Google Scholar 

  77. Tesfaigzi J, Wright PS, Oreffo V, An G, Wu R, Carlson DM (1993) A small proline-rich protein regulated by vitamin A in tracheal epithelial cells is induced in lung tumors. Am J Respir Cell Mol Biol 9(4):434–440. doi:10.1165/ajrcmb/9.4.434

    Article  PubMed  CAS  Google Scholar 

  78. Tesfaigzi Y, Wright PS, Belinsky SA (2003) SPRR1B overexpression enhances entry of cells into the G0 phase of the cell cycle. Am J Physiol Lung Cell Mol Physiol 285(4):L889–L898. doi:10.1152/ajplung.00065.2003

    PubMed  CAS  Google Scholar 

  79. Tong L, Corrales RM, Chen Z, Villarreal AL, De Paiva CS, Beuerman R, Li DQ, Pflugfelder SC (2006) Expression and regulation of cornified envelope proteins in human corneal epithelium. Invest Ophthalmol Vis Sci 47(5):1938–1946. doi:10.1167/iovs.05-1129

    Article  PubMed  Google Scholar 

  80. Vermeij WP, Backendorf C (2010) Skin cornification proteins provide global link between ROS detoxification and cell migration during wound healing. PLoS One 5(8):e11957. doi:10.1371/journal.pone.0011957

    Article  PubMed  Google Scholar 

  81. Vermeij WP, Florea BI, Isenia S, Alia A, Brouwer J, Backendorf C (2012) Proteomic Identification of in Vivo Interactors Reveals Novel Function of Skin Cornification Proteins. J Proteome Res. doi:10.1021/pr300310b

    PubMed  Google Scholar 

  82. Yaar M, Eller MS, Bhawan J, Harkness DD, DiBenedetto PJ, Gilchrest BA (1995) In vivo and in vitro SPRR1 gene expression in normal and malignant keratinocytes. Exp Cell Res 217(2):217–226. doi:10.1006/excr1995.1081

    Article  PubMed  CAS  Google Scholar 

  83. Zhang Y, Feng YB, Shen XM, Chen BS, Du XL, Luo ML, Cai Y, Han YL, Xu X, Zhan QM, Wang MR (2008) Exogenous expression of Esophagin/SPRR3 attenuates the tumorigenicity of esophageal squamous cell carcinoma cells via promoting apoptosis. Int J Cancer J Int du Cancer 122(2):260–266. doi:10.1002/ijc.23104

    Article  CAS  Google Scholar 

  84. Zimmermann N, Doepker MP, Witte DP, Stringer KF, Fulkerson PC, Pope SM, Brandt EB, Mishra A, King NE, Nikolaidis NM, Wills-Karp M, Finkelman FD, Rothenberg ME (2005) Expression and regulation of small proline-rich protein 2 in allergic inflammation. Am J Respir Cell Mol Biol 32(5):428–435. doi:10.1165/rcmb.2004-0269OC

    Article  PubMed  CAS  Google Scholar 

  85. Zinovyeva MV, Monastyrskaya GS, Kopantzev EP, Vinogradova TV, Kostina MB, Sass AV, Filyukova OB, Uspenskaya NY, Sukhikh GT, Sverdlov ED (2010) Identification of some human genes oppositely regulated during esophageal squamous cell carcinoma formation and human embryonic esophagus development. Dis Esophagus Off J Int Soc Dis Esophagus/ISDE 23(3):260–270. doi:10.1111/j.1442-2050.2009.01008.x

    Article  CAS  Google Scholar 

  86. Zucchini C, Strippoli P, Rosati G, Del Governatore M, Milano E, Ugolini G, Solmi R, Mattei G, Caira A, Zanotti S, Carinci P, Valvassori L (2000) Expression analysis and mutational screening of the epithelium-specific ets gene-1 (ESE-1) in patients with squamous anal cancer. Int J Oncol 17(2):265–270

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank the Fundação de Amparo à Pesquisa do Estado de São Paulo/FAPESP, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior/CAPES and Conselho Nacional de Pesquisas/CNPq for financial support and fellowships. They are also grateful to Professor Sergio Russo Matioli (Bioscience Institute, University of São Paulo/USP) and to the GENCAPO (Head and Neck Genome Project—http://www.gencapo.famerp.br/) team for the valuable discussions that motivated the present study.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Genetics and Evolutionary Biology, Institute of Biosciences, University of São Paulo, São Paulo, São Paulo, Brazil

    Fernanda Carregaro & Eloiza H. Tajara

  2. Department of Molecular Biology, School of Medicine of São José do Rio Preto, FAMERP, Av. Brigadeiro Faria Lima, 5416, Vila São Pedro, São José do Rio Preto, São Paulo, 15090-000, Brazil

    Fernanda Carregaro, Ana Carolina B. Stefanini, Tiago Henrique & Eloiza H. Tajara

Authors
  1. Fernanda Carregaro
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ana Carolina B. Stefanini
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tiago Henrique
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Eloiza H. Tajara
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Eloiza H. Tajara.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Carregaro, F., Stefanini, A.C.B., Henrique, T. et al. Study of small proline-rich proteins (SPRRs) in health and disease: a review of the literature. Arch Dermatol Res 305, 857–866 (2013). https://doi.org/10.1007/s00403-013-1415-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00403-013-1415-9

Keywords

Search

Navigation