Structure-activity analysis of histatin, a potent wound healing peptide from human saliva: Cyclization of histatin potentiates molar activity 1000-fold

FASEB Journal

Volumn 23, Issue 11, 2009, Pages 3928-3935

  Oudhoff, Menno J ^a   Kroeze, Kim L ^b   Nazmi, Kamran ^a   Van Den Keijbus, Petra A M ^a   Van 't Hof, Wim ^a   Fernandez Borja, Mar ^a   Hordijk, Peter L ^a   Gibbs, Susan ^b   Bolscher, Jan G M ^a   Veerman, Enno C I ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Antimicrobial peptides; Cell migration; Cyclic peptide; Domain mapping; Reepithelialization

Indexed keywords

G PROTEIN COUPLED RECEPTOR; HISTATIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3;

ARTICLE; CELL ACTIVATION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; CYCLIZATION; ENZYME ACTIVATION; EPITHELIZATION; HUMAN; HUMAN CELL; MOUTH MUCOSA; PRIORITY JOURNAL; SALIVA; STRUCTURE ACTIVITY RELATION; WOUND; WOUND HEALING;

AMINO ACID SEQUENCE; CELL MOVEMENT; CELL PROLIFERATION; CYCLIZATION; DRUG SYNERGISM; HISTATINS; HUMANS; INFANT, NEWBORN; KERATINOCYTES; MALE; MODELS, BIOLOGICAL; SALIVA; STRUCTURE-ACTIVITY RELATIONSHIP; WOUND HEALING;

EID: 70350548183     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.09-137588     Document Type: Article

References (40)

1. Vissink, A., Jansma, J., Spijkervet, F. K., Burlage, F. R., and Coppes, R. P. (2003) Oral sequelae of head and neck radiotherapy. Crit. Rev. Oral Biol. Med. 14, 199-212 (Pubitemid 44560804)
2. Denny, P., Hagen, F. K., Hardt, M., Liao, L., Yan, W., Arellanno, M., Bassilian, S., Bedi, G. S., Boontheung, P., Cociorva, D., Delahunty, C. M., Denny, T., Dunsmore, J., Faull, K. F., Gilligan, J., Gonzalez-Begne, M., Halgand, F., Hall, S. C., Han, X., Henson, B., Hewel, J., Hu, S., Jeffrey, S., Jiang, J., Loo, J. A., Ogorzalek Loo, R. R., Malamud, D., Melvin, J. E., Miroshnychenko, O., Navazesh, M., Niles, R., Park, S. K., Prakobphol, A., Ramachandran, P., Richert, M., Robinson, S., Sondej, M., Souda, P., Sullivan, M. A., Takashima, J., Than, S., Wang, J., Whitelegge, J. P., Witkowska, H. E., Wolinsky, L., Xie, Y., Xu, T., Yu, W., Ytterberg, J., Wong, D. T., Yates, J. R., 3rd, and Fisher, S. J. (2008) The proteomes of human parotid and submandibular/sublingual gland salivas collected as the ductal secretions. J. Proteome Res. 7, 1994-2006
3. Engeland, C. G., Bosch, J. A., Cacioppo, J. T., and Marucha, P. T. (2006) Mucosal wound healing: the roles of age and sex. Arch. Surg. 141, 1193-1197; discussion 1198
4. Kiecolt-Glaser, J. K., Marucha, P. T., Malarkey, W. B., Mercado, A. M., and Glaser, R. (1995) Slowing of wound healing by psychological stress. Lancet 346, 1194-1196
5. Szpaderska, A. M., Zuckerman, J. D., and DiPietro, L. A. (2003) Differential injury responses in oral mucosal and cutaneous wounds. J. Dent. Res. 82, 621-626
6. Hutson, J. M., Niall, M., Evans, D., and Fowler, R. (1979) Effect of salivary glands on wound contraction in mice. Nature 279, 793-795 (Pubitemid 9202556)
7. Konturek, S. J., Dembinski, A., Warzecha, Z., Brzozowski, T., and Gregory, H. (1988) Role of epidermal growth factor in healing of chronic gastroduodenal ulcers in rats. Gastroenterology 94, 1300-1307 (Pubitemid 18153628)
8. Fisher, D. A., and Lakshmanan, J. (1990) Metabolism and effects of epidermal growth factor and related growth factors in mammals. Endocr. Rev. 11, 418-442 (Pubitemid 20261694)
9. Murphy, R. A., Watson, A. Y., Metz, J., and Forssmann, W. G. (1980) The mouse submandibular gland: an exocrine organ for growth factors. J. Histochem. Cytochem. 28, 890-902 (Pubitemid 11253579)
10. Oudhoff, M. J., Bolscher, J. G., Nazmi, K., Kalay, H., van 't Hof, W., Amerongen, A. V., and Veerman, E. C. (2008) Histatins are the major wound-closure stimulating factors in human saliva as identified in a cell culture assay. FASEB J. 22, 3805-3812
11. Sun, X., Salih, E., Oppenheim, F. G., and Helmerhorst, E. J. (2009) Kinetics of histatin proteolysis in whole saliva and the effect on bioactive domains with metal-binding, antifungal, and wound-healing properties. [E-pub ahead of print] FASEB J. doi: 10/1096/fj.09-131045
12. Baum, B. J., Bird, J. L., Millar, D. B., and Longton, R. W. (1976) Studies on histidine-rich polypeptides from human parotid saliva. Arch. Biochem. Biophys. 177, 427-436 (Pubitemid 8012812)
13. Oppenheim, F. G., Xu, T., McMillian, F. M., Levitz, S. M., Diamond, R. D., Offner, G. D., and Troxler, R. F. (1988) Histatins, a novel family of histidine-rich proteins in human parotid secretion. Isolation, characterization, primary structure, and fungistatic effects on Candida albicans. J. Biol. Chem. 263, 7472-7477 (Pubitemid 18147029)
14. Ruissen, A. L., Groenink, J., Van't Hof, W., Walgreen-Weterings, E., van Marle, J., van Veen, H. A., Voorhout, W. F., Veerman, E. C., and Nieuw Amerongen, A. V. (2002) Histatin 5 and derivatives. Their localization and effects on the ultra-structural level. Peptides 23, 1391-1399
15. Veerman, E. C., Valentijn-Benz, M., Nazmi, K., Ruissen, A. L., Walgreen-Weterings, E., van Marle, J., Doust, A. B., van't Hof, W., Bolscher, J. G., and Nieuw Amerongen, A. V. (2007) Energy depletion protects Candida albicans against antimicrobial peptides by rigidifying its cell membrane. J. Biol. Chem. 282, 18831-18841
16. Mochon, A. B., and Liu, H. (2008) The antimicrobial peptide histatin-5 causes a spatially restricted disruption on the Candida albicans surface, allowing rapid entry of the peptide into the cytoplasm. PLoS Pathog 4, e1000190
17. Gibbs, S., van den Hoogenband, H. M., Kirtschig, G., Richters, C. D., Spiekstra, S. W., Breetveld, M., Scheper, R. J., and de Boer, E. M. (2006) Autologous full-thickness skin substitute for healing chronic wounds. Br. J. Dermatol. 155, 267-274 (Pubitemid 44050558)
18. Stawikowski, M., and Cudic, P. (2006) A novel strategy for the solid-phase synthesis of cyclic lipodepsipeptides. Tetrahedron. Lett. 47, 8587-8590 (Pubitemid 44634600)
19. Ponec, M., Kempenaar, J. A., and De Kloet, E. R. (1981) Corticoids and cultured human epidermal keratinocytes: specific intracellular binding and clinical efficacy. J. Invest. Dermatol. 76, 211-214 (Pubitemid 11114065)
20. Breetveld, M., Richters, C. D., Rustemeyer, T., Scheper, R. J., and Gibbs, S. (2006) Comparison of wound closure after burn and cold injury in human skin equivalents. J. Invest. Dermatol. 126, 1918-1921 (Pubitemid 44086530)
21. Abramoff, M. D., Magelhaes, P. J., and Ram, S. J. (2004) Image processing with ImageJ. Biophotonics International 11, 26-42
22. Lorenowicz, M. J., Fernandez-Borja, M., van Stalborch, A. M., van Sterkenburg, M. A., Hiemstra, P. S., and Hordijk, P. L. (2007) Microtubule dynamics and Rac-1 signaling independently regulate barrier function in lung epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 293, L1321-L1331 (Pubitemid 350159417)
23. Brennand, D. M., Dennehy, U., Ellis, V., Scully, M. F., Tripathi, P., Kakkar, V. V., and Patel, G. (1997) Identification of a cyclic peptide inhibitor of platelet-derived growth factor-BB receptor-binding and mitogen-induced DNA synthesis in human fibroblasts. FEBS Lett. 413, 70-74 (Pubitemid 27348639)
24. Yokoyama, F., Suzuki, N., Haruki, M., Nishi, N., Oishi, S., Fujii, N., Utani, A., Kleinman, H. K., and Nomizu, M. (2004) Cyclic peptides from the loop region of the laminin alpha 4 chain LG4 module show enhanced biological activity over linear peptides. Biochemistry 43, 13590-13597 (Pubitemid 39391159)
25. Jackson, S., DeGrado, W., Dwivedi, A., Parthasarathy, A., Higley, A., Krywko, J., Rockwell, A., Markwalder, J., and Wells, G. (1994) Template-constrained cyclic peptides: design of high-affinity ligands for GPIIb/IIIa. J. Amer. Chem. Soc. 116, 3220-3230 (Pubitemid 24165237)
26. Zhou, N., Luo, Z., Luo, J., Fan, X., Cayabyab, M., Hiraoka, M., Liu, D., Han, X., Pesavento, J., Dong, C. Z., Wang, Y., An, J., Kaji, H., Sodroski, J. G., and Huang, Z. (2002) Exploring the stereochemistry of CXCR4-peptide recognition and inhibiting HIV-1 entry with D-peptides derived from chemokines. J. Biol. Chem. 277, 17476-17485 (Pubitemid 34967547)
27. Tang, Y. Q., Yuan, J., Osapay, G., Osapay, K., Tran, D., Miller, C. J., Ouellette, A. J., and Selsted, M. E. (1999) A cyclic antimicrobial peptide produced in primate leukocytes by the ligation of two truncated alpha-defensins. Science 286, 498-502
28. Garcia, A. E., Osapay, G., Tran, P. A., Yuan, J., and Selsted, M. E. (2008) Isolation, synthesis, and antimicrobial activities of naturally occurring theta-defensin isoforms from baboon leukocytes. Infect. Immun. 76, 5883-5891
29. Huang, R. P., Wu, J. X., Fan, Y., and Adamson, E. D. (1996) UV activates growth factor receptors via reactive oxygen intermediates. J. Cell Biol. 133, 211-220 (Pubitemid 26107108)
30. Niyonsaba, F., Ushio, H., Nakano, N., Ng, W., Sayama, K., Hashimoto, K., Nagaoka, I., Okumura, K., and Ogawa, H. (2007) Antimicrobial peptides human beta-defensins stimulate epidermal keratinocyte migration, proliferation and production of proinflammatory cytokines and chemokines. J. Invest. Dermatol. 127, 594-604 (Pubitemid 46271027)
31. Tjabringa, G. S., Aarbiou, J., Ninaber, D. K., Drijfhout, J. W., Sorensen, O. E., Borregaard, N., Rabe, K. F., and Hiemstra, P. S. (2003) The antimicrobial peptide LL-37 activates innate immunity at the airway epithelial surface by transactivation of the epidermal growth factor receptor. J. Immunol. 171, 6690-6696 (Pubitemid 37532101)
32. Xu, K. P., Yin, J., and Yu, F. S. (2007) Lysophosphatidic acid promoting corneal epithelial wound healing by transactivation of epidermal growth factor receptor. Invest. Ophthalmol. Vis. Sci. 48, 636-643 (Pubitemid 351260695)
33. Tokumaru, S., Sayama, K., Shirakata, Y., Komatsuzawa, H., Ouhara, K., Hanakawa, Y., Yahata, Y., Dai, X., Tohyama, M., Nagai, H., Yang, L., Higashiyama, S., Yoshimura, A., Sugai, M., and Hashimoto, K. (2005) Induction of keratinocyte migration via transactivation of the epidermal growth factor receptor by the antimicrobial peptide LL-37. J. Immunol. 175, 4662-4668 (Pubitemid 41362007)
34. Zlotnik, A., Yoshie, O., and Nomiyama, H. (2006) The chemokine and chemokine receptor superfamilies and their molecular evolution. Genome Biol. 7, 243 (Pubitemid 46995589)
35. Von Haussen, J., Koczulla, R., Shaykhiev, R., Herr, C., Pinkenburg, O., Reimer, D., Wiewrodt, R., Biesterfeld, S., Aigner, A., Czubayko, F., and Bals, R. (2008) The host defence peptide LL-37/hCAP-18 is a growth factor for lung cancer cells. Lung Cancer 59, 12-23
36. Johansson, J., Gudmundsson, G. H., Rottenberg, M. E., Berndt, K. D., and Agerberth, B. (1998) Conformation-dependent antibacterial activity of the naturally occurring human peptide LL-37. J. Biol. Chem. 273, 3718-3724 (Pubitemid 28109800)
37. Aarbiou, J., Tjabringa, G. S., Verhoosel, R. M., Ninaber, D. K., White, S. R., Peltenburg, L. T., Rabe, K. F., and Hiemstra, P. S. (2006) Mechanisms of cell death induced by the neutrophil antimicrobial peptides alpha-defensins and LL-37. Inflamm. Res. 55, 119-127
38. Van Wetering, S., Mannesse-Lazeroms, S. P., Dijkman, J. H., and Hiemstra, P. S. (1997) Effect of neutrophil serine proteinases and defensins on lung epithelial cells: modulation of cytotoxicity and IL-8 production. J. Leukoc. Biol. 62, 217-226 (Pubitemid 27380794)
39. Barrientos, S., Stojadinovic, O., Golinko, M. S., Brem, H., and Tomic-Canic, M. (2008) Growth factors and cytokines in wound healing. Wound Repair Regen. 16, 585-601
40. Occleston, N. L., O'Kane, S., Goldspink, N., and Ferguson, M. W. (2008) New therapeutics for the prevention and reduction of scarring. Drug Discov. Today 13, 973-981