Hyaluronic acid and skin: Wound healing and aging

International Journal of Dermatology

Volumn 35, Issue 8, 1996, Pages 539-544

  Manuskiatti, Woraphong ^a   Maibach, Howard I ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYALURONIC ACID; RETINOIC ACID;

AGED; AGING; HUMAN; REVIEW; SKIN INJURY; TOPICAL DRUG ADMINISTRATION; WOUND HEALING;

EID: 0029785697     PISSN: 00119059     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-4362.1996.tb03650.x     Document Type: Review

References (82)

1. Meyer K, Palmer JW. The polysaccharide of the vitreous humor. J Biol Chem 1934; 107:629-634.
2. Reed RK, Laurent UB. Turnover of hyaluronan in the microcirculation. Am Rev Respir Dis 1992; 146:S37-S39.
3. Laurent TC. Hyaluronan - an introduction. In: Willoughby DA, ed. Second International Workshop on hyaluronan in drug delivery. Toronto, Ontario, Canada: Royal Society of Medicine Press, 1995:2-4.
4. Goa KL, Benfield P. Hyaluronic acid. A review of its pharmacology and use as a surgical aid in ophthalmology and its therapeutic potential in joint disease and wound healing. Drugs 1994; 47:536-566.
5. Laurent TC, Fraser JR. Hyaluronan. FASEB J 1992; 6: 2397-2404.
6. Toole BP. Hyaluronan and its binding proteins, the hyaladherins. Curr Opin Cell Biol 1990; 2:839-844.
7. Bertolami CN, Berg S, Messadi DV. Binding and internalization of hyaluronate by human cutaneous fibroblasts. Matrix 1992; 12:11-21.
8. Reed RK, Lilja K, Laurent TC. Hyaluronan in the rat with special reference to the skin. Acta Physiol Scand 1988; 134:405-411.
9. Akiyama H, Saito M, Qiu G, et al. Analytical studies on hyaluronic acid synthesis by normal human epidermal keratinocytes cultured in a serum-free medium. Biol Pharm Bull 1994; 17:361-364.
10. Tammi R, Ripellino JA, Margolis RU, et al. Hyaluronate accumulation in human epidermis treated with retinoic acid in skin organ culture. J Invest Dermatol 1989; 92:326-332.
11. Tammi R, Tammi M. Influence of retinoic acid on the ultrastructure and hyaluronic acid synthesis of adult human epidermis in whole skin organ culture. J Cell Physiol 1986; 126:389-398.
12. Tammi R, Jansen CT, Tammi M. Effects of retinoic acid on adult human epidermis in whole skin organ culture. Arch Dermatol Res 1985; 277:276-283.
13. King IA. Increased epidermal hyaluronic acid synthesis caused by four retinoids. Br J Dermatol 1984; 110: 607-608.
14. Uzuka M, Nakajima K, Ohta S, Mori Y. The mechanism of estrogen-induced increase in hyaluronic acid biosynthesis, with special reference to estrogen receptor in the mouse skin. Biochim Biophys Acta 1980; 627:199-206.
15. Edward M, Oliver RF. Changes in the synthesis, distribution and sulphation of glycosaminoglycans of cultured human skin fibroblasts upon ascorbate feeding. J Cell Sci 1983; 64:245-254.
16. Saarni H, Tammi M, Doherty NS. Decreased hyaluronic acid synthesis, a sensitive indicator of cortisol action on fibroblast. J Pharm Pharmacol 1978; 30:200-201.
17. Saarni H, Hopsu-Havu VK. The decrease of hyaluronate synthesis by anti-inflammatory steroids in vitro. Br J Dermatol 1978; 98:445-449.
18. Saarni H, Jalkanen M, Hopsu-Havu VK. Effect of five anti-inflammatory steroids on collagen and glycoaminoglycan synthesis in vitro. Br J Dermatol 1980; 103:167-173.
19. Meyer LJ, Stern R. Age-dependent changes of hyaluronan in human skin. J Invest Dermatol 1994; 102:385-389.
20. Brecht M, Mayer U, Schlosser E, Prehm P. Increased hyaluronate synthesis is required for fibroblast detachment and mitosis. Biochem J 1986; 239:445-450.
21. Mian N. Analysis of cell-growth-phase-related variations in hyaluronate synthase activity of isolated plasmamembrane fractions of cultured human skin fibroblasts. Biochem J 1986; 237:333-342.
22. Barnhart BJ, Cox SH, Kraemer PM. Detachment variants of Chinese hamster cells. Hyaluronic acid as a modulator of cell detachment. Exp Cell Res 1979; 119: 327-332.
23. Lamberg SI, Yuspa SH, Hascall VC. Synthesis of hyaluronic acid is decreased and synthesis of proteoglycans is increased when cultured mouse epidermal cells differentiate. J Invest Dermatol 1986; 86:659-667.
24. Tammi R, Ripellino JA, Margolis RU, Tammi M. Localization of epidermal hyaluronic acid using the hyaluronate binding region of cartilage proteoglycan as a specific probe. J Invest Dermatol 1988; 90:412-414.
25. Moczar M, Robert L. Stimulation of cell proliferation by hyaluronidase during in vitro aging of human skin fibroblasts. Exp Gerontol 1993; 28:59-68.
26. Ghersetich I, Lotti T, Campanile G, et al. Hyaluronic acid in cutaneous intrinsic aging. Int J Dermatol 1994; 33:119-122.
27. Laurent TC, Fraser JR. The properties and turnover of hyaluronan. Ciba Found Symp 1986; 124:9-29.
28. Yoneda M, Suzuki S, Kimata K. Hyaluronic acid associated with the surfaces of cultured fibroblasts is linked to a serum-derived 85-kDa protein. J Biol Chem 1990; 265:5247-5257.
29. Banerjee SD, Toole BP. Monoclonal antibody to chick embryo hyaluronan-binding protein: changes in distribution of binding protein during early brain development. Dev Biol 1991; 146:186-197.
30. LeBoeuf RD, Raja RH, Fuller GM, Weigel PH. Human fibrinogen specifically binds hyaluronic acid. J Biol Chem 1986; 261:12586-12592.
31. Burd DA, Siebert JW, Ehrlich HP, Garg HG. Human skin and post-burn scar hyaluronan: demonstration of the association with collagen and other proteins. Matrix 1989; 9:322-327.
32. Kielty CM, Whittaker SP, Grant ME, Shuttleworth CA. Type VI collagen microfibrils: evidence for a structural association with hyaluronan. J Cell Biol 1992; 118: 979-990.
33. Kielty CM, Whittaker SP, Grant ME, Shuttleworth CA. Type VI collagen forms a structural association with hyaluronan in vivo. Biochem Soc Trans 1991; 19:384S.
34. McDevitt CA, Marcelino J, Tucker L. Interaction of intact type VI collagen with hyaluronan. FEBS Lett 1991; 294: 167-170.
35. Culty M, Miyake K, Kincade PW, et al. The hyaluronate receptor is a member of the CD44 (H-CAM) family of cell surface glycoproteins. J Cell Biol 1990; 111:2765-2774. [published erratum appears in: J Cell Biol 1991; 112:513.]
36. Yasaka N, Furue M, Tamaki K. CD44 expression in normal human skin and skin tumors. J Dermatol 1995; 22:88-94.
37. Underhill CB. Hyaluronan is inversely correlated with the expression of CD44 in the dermal condensation of the embryonic hair follicle. J Invest Dermatol 1993; 101:820-826.
38. Wang C, Tammi M, Tammi R. Distribution of hyaluronan and its CD44 receptor in the epithelia of human skin appendages. Histochemistry 1992; 98:105-112.
39. Hardwick C, Hoare K, Owens R, et al. Molecular cloning of a novel hyaluronan receptor that mediates tumor cell motility. J Cell Biol 1992; 117:1343-1350. [published erratum appears in: J Cell Biol 1992; 118(3):753.]
40. Yang B, Hall CL, Yang BL, et al. Identification of a novel heparin-binding domain in RHAMM and evidence that it modifies HA-mediated locomotion of ras-transformed cells. J Cell Biochem 1994; 56:455-468.
41. Yang B, Yang BL, Savani RC, Turley EA. Identification of a common hyaluronan-binding motif in the hyaluronan-binding proteins RHAMM, CD44 and link protein. Embo J 1994; 13:286-296.
42. Krummel TM, Nelson JM, Diegelmann RF, et al. Fetal response to injury in the rabbit. J Pediatr Surg 1987; 22:640-644.
43. DePalma RL, Krummel TM, Nelson JM, et al. Fetal wound matrix is composed of proteoglycan rather collagen. Surg Forum 1987; 38:626-628.
44. Alaish SM, Yager D, Diegelmann RF, Cohen IK. Biology of fetal wound healing: hyaluronate receptor expression in fetal fibroblasts. J Pediatr Surg 1994; 29:1040-1043.
45. Longaker MT, Adzick NS, Hall JL, et al. Studies in fetal wound healing. VII. Fetal wound healing may be modulated by hyaluronic acid-stimulating activity in amniotic fluid. J Pediatr Surg 1990; 25:430-433.
46. Mast BA, Diegelmann RF, Krummel TM, Cohen IK. Hyaluronic acid modulates proliferation, collagen and protein synthesis of cultured fetal fibroblasts. Matrix 1993; 13:441-446.
47. Mast BA, Haynes JH, Krummel TM, et al. In vivo degradation of fetal wound hyaluronic acid results in increased fibroplasia, collagen deposition, and neovascularization. Plast Reconstr Surg 1992; 89:503-509.
48. Hellstrom S, Laurent C. Hyaluronan and healing of tympanic membrane perforations. An experimental study. Acta Otolaryngol [Suppl] 1987; 442:54-61.
49. Bertheim U, Hellstrom S. The distribution of hyaluronan in human skin and mature, hypertrophic and keloid scars. Br J Plast Surg 1994; 47:483-489.
50. Passarini B, Tosti A, Fanti PA, Varotti C. [Effect of hyaluronic acid on the reparative process of non-healing ulcers. Comparative study]. G Ital Dermatol Venereol 1982; 117:27-30. [Italian]
51. Torregrossa F, Caroti A. [Clinical verification of the use of topical hyaluronic acid under non-adhesive gauze in the therapy of torpid ulcers]. G Ital Dermatol Venereol 1983; 118:41-44. [Italian]
52. Venturini D. [Clinical observations on the use of hyaluronic acid in dermatologie therapy]. G Ital Dermatol Venereol 1985; 120:5-10. [Italian]
53. Celleno L, Piperno S, Bracaglia R. [Clinico-experimental studies on the use of hyaluronic acid in skin healing processes. Preliminary data]. G Ital Dermatol Venereol 1985; 120:47-56. [Italian]
54. Retanda G. [Hyaluronic acid in the process of reparation of cutaneous ulcers. Clinical experience]. G Ital Dermatol Venereol 1985; 120:71-75. [Italian]
55. Abatangelo G, Martelli M, Vecchia P. Healing of hyaluronic acid-enriched wounds: histological observations. J Surg Res 1983; 35:410-416.
56. Trabucchi E, Preis Baruffaldi F, Baratti C, Montorsi W. Topical treatment of experimental skin lesions in rats: macroscopic, microscopic and scanning electron-microscopic evaluation of the healing process. Int J Tissue React 1986; 8:533-544.
57. King SR, Hickerson WL, Proctor KG. Beneficial actions of exogenous hyaluronic acid on wound healing. Surgery 1991; 109:76-84.
58. Doillon CJ, Dunn MG, Berg RA, Silver FH. Collagen deposition during wound repair. Scanning Electron Microsc 1985; 2:897-903.
59. Doillon CJ, Silver FH. Collagen-based wound dressing: effects of hyaluronic acid and fibronectin on wound healing. Biomaterials 1986; 7:3-8.
60. Burd DA, Greco RM, Regauer S, et al. Hyaluronan and wound healing: a new perspective. Br J Plast Surg 1991; 44:579-584.
61. Laurent C, Hellstrom S, Fellenius E. Hyaluronan improves the healing of experimental tympanic membrane perforations. A comparison of preparations with different rheologic properties. Arch Otolaryngol Head Neck Surg 1988; 114:1435-1441.
62. Toole BP, Munaim SI, Welles S, Knudson CB. Hyaluronate-cell interactions and growth factor regulation of hyaluronate synthesis during limb development. Ciba Found Symp 1989; 143:138-145, discussion 145-149, 281-285.
63. Sarnstrand B, Brattsand R, Malmstrom A. Effect of glucocorticoids on glycosaminoglycan metabolism in cultured human skin fibroblasts. J Invest Dermatol 1982; 79:412-417.
64. Fleischmajer R, Perlish JS, Bashey RI. Aging of human dermis. In: Robert CL, ed. Frontiers of Matrix Biology. Vol. 1. Basel: Karger, 1973:90.
65. Fleischmajer R, Perlish JS, Bashey RI. Human dermal glycosaminoglycans and aging. Biochim Biophys Acta 1972; 279:265-275.
66. Breen M, Weinstein HG, Blacik LJ, Borcherding MS. Microanalysis and characterization of glycosaminoglycans from human tissue via zone electrophoresis. In: Whistler RL, BeMiller JN, eds. Methods in carbohydrate chemistry. New York: Academic Press, 1976: 101-115.
67. Schachtschabel DO, Wever J. Age-related decline in the synthesis of glycosaminoglycans by cultured human fibroblasts (WI-38). Mech Ageing Dev 1978; 8:257-264.
68. Sluke G, Schachtschabel DO, Wever J. Age-related changes in the distribution pattern of glycosaminoglycans synthesized by cultured human diploid fibroblasts (WI-38). Mech Ageing Dev 1981; 16:19-27.
69. Willen MD, Sorrell JM, Lekan CC, et al. Patterns of glycosaminoglycan/proteoglycan immunostaining in human skin during aging. J Invest Dermatol 1991; 96:968-974.
70. Poulsen JH, Cramers MK. Determination of hyaluronic acid, dermatan sulphate, heparan sulphate and chondroitin 4/6 sulphate in human dermis, and a material of reference. Scand J Clin Lab Invest 1982; 42:545-549.
71. Ghersetich I, Teofoli P, Benci M, Lotti T. Ultrastructural study of hyaluronic acid before and after the use of a pulsed electromagnetic field, electrorydesis, in the treatment of wrinkles. Int J Dermatol 1994; 33:661-663.
72. Miyamoto I, Nagase S. Age-related changes in the molecular weight of hyaluronic acid from rat skin. Jikken Dobutsu 1984; 33:481-485.
73. Lundin F, BB, GM. Topical retinoic acid treatment of photoaged skin: its effects on hyaluronan distribution in epidermis and on hyaluronan and retinoic acid in suction blister fluid. Acta Derm Venereol Scand 1992; 72:423-427.
74. Fuchs E, Green H. Regulation of terminal differentiation of cultured human keratinocytes by vitamin A. Cell 1981; 25:617-625.
75. Tanaka S. Changes in morphology and cell proliferation during vitamin A-induced mucous metaplasia of developing chick scale cultured in vitro. J Exp Zool 1982; 223:139-154.
76. Yuspa SH, Harris CC. Altered differentiation of mouse epidermal cells treated with retinyl acetate in vitro. Exp Cell Res 1974; 86:95-105.
77. Barnett ML, Szabo G. Effect of vitamin A on epithelial morphogenesis in vitro. Exp Cell Res 1973; 76:118-126.
78. Elias PM, Fritsch PO, Lampe M, et al. Retinoid effects on epidermal structure, differentiation, and permeability. Lab Invest 1981; 44:531-540.
79. Milstone LM, McGuire J, LaVigne JF. Retinoic acid causes premature desquamation of cells from confluent cultures of stratified squamous epithelia. J Invest Dermatol 1982; 79:253-260.
80. Kanerva L, Lauharanta J, Niemi KM, Lassus A. New observations on the fine structure of lamellar ichthyosis and the effect of treatment with etretinate. Am J Dermatopathol 1983; 5:555-568.
81. Gilfix BM, Eckert RL. Coordinate control by vitamin A of keratin gene expression in human keratinocytes. J Biol Chem 1985; 260:14026-14029.
82. Kopan R, Traska G, Fuchs E. Retinoids as important regulators of terminal differentiation: examining keratin expression in individual epidermal cells at various stages of keratinization. J Cell Biol 1987; 105:427-440.