Cysteine proteases: Mode of action and role in epidermal differentiation

Cell and Tissue Research

Volumn 351, Issue 2, 2013, Pages 237-244

  Brocklehurst, Keith ^a   Philpott, Mike P ^b  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Caspases; Cathepsins; Cornification; Cystatin M E; Cysteine proteases; Desquamation; Epidermis

Indexed keywords

CASPASE; CATHEPSIN; CYSTATIN; CYSTATIN M; CYSTEINE PROTEINASE; STEFIN A;

CELL DIFFERENTIATION; DESQUAMATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME MECHANISM; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SQUAMOUS EPITHELIUM; ANIMAL; CYTOLOGY; ENZYMOLOGY; EPIDERMIS; METABOLISM; PHYSIOLOGY;

MAMMALIA;

ANIMALS; CELL DIFFERENTIATION; CYSTEINE PROTEASES; EPIDERMIS; HUMANS;

EID: 84891475036     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-013-1557-2     Document Type: Review

References (80)

1. Abrahamson M, Alvarez-Fernandez M, Nathanson CM (2003) Cystatins. Biochem Soc Symp 70:179-199
2. Akgül B, Cooke JC, Storey A (2006) HPV-associated skin disease. J Pathol 208:165-175
3. Barrett AJ, Rawlings ND, Woessner JF (2004) Handbook of proteolytic enzymes. Elsevier, London
4. Benavides F, Starost MF, Flores M, Gimenez-Conti IB, Guenet JL, Conti CJ (2002) Impaired hair follicle morphogenesis and cycling with abnormal epidermal differentiation in nackt mice, a cathepsin L-deficient mutation. Am J Pathol 161:693-703
5. Blaydon DC, Nitoiu D, Eckl KM, Cabral RM, Bland P, Hausser I, Heel DA van, Rajpopat S, Fischer J, Oji V, Zvulunov A, Traupe H, Hennies HC, Kelsell DP (2011) Mutations in CSTA, encoding Cystatin A, underlie exfoliative ichthyosis and reveal a role for this protease inhibitor in cell-cell adhesion. Am J Hum Genet 89:564-571
6. Brocklehurst K (1982) Twoprotonic-state electrophiles as probes of enzyme mechanism. Methods Enzymol 87:427-469
7. Brocklehurst K (1994) A sound basis for pH-dependent kinetic studies on enzymes. Protein Eng 7:291-299
8. Brocklehurst K, Little G (1970) A novel reactivity of papain and a convenient active site titration in the presence of other thiols. FEBS Lett 9:113-116
9. Brocklehurst K, Carlsson J, Kierston MPJ, Crook EM (1973) Covalent chromatography: preparation of fully active papain from dried papaya latex. Biochem J 133:573-584
10. Brocklehurst K, Carlsson J, Kierston MPJ, Crook EM (1974) Covalent chromatography by thiol-disulphide interchange. Methods Enzymol 34:531-544
11. Brocklehurst K, Carey PR, Lee H, Salih E, Storer AC (1984) Comparative resonance Raman spectroscopic and kinetic studies of acyl enzymes involving papain, actinidin and papaya peptidase II. Biochem J 233:649-657
12. Brocklehurst K, Willenbrook F, Salih E (1987) Cysteine proteinases. In: Neuberger A, Brocklehurst K (eds) Hydrolytic enzymes. New comprehensive biochemistry, vol 16. Elsevier, Amsterdam, pp 39-158
13. Brocklehurst K, Watts AB, Patel M, Verma C, Thomas EW (1998) Cysteine proteinases. In: Sinnott ML (ed) Comprehensive biological catalysis, vol 1. Academic Press, London, pp 381-423
14. Brocklehurst K, Courey AJ, Gul S, Lin S-H, Moritz RL (2004) Affinity and immunoaffinity chromatography. In: Simpson RJ (ed) Purifying proteins for proteomics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp 221-273
15. Brocklehurst K, Gul S, Pickersgill RW (2009) Substrate recognition. In: Hughes AB (ed) Amino acids peptides and proteins in organic chemistry, vol 2. Modified amino acids organocatalysis and enzymes. Wiley VCH, Weinheim, pp 473-504
16. Candi E, Schmidt R, Melina G (2005) The cornified envelope: a model of cell death in the skin. Nat Rev Mol Cell Biol 6:328-340
17. Cheng T, Hitomi K, Ivonne MJ, Van Wlijmen-Willems J, Le Jongh GJ, Yamamoto K, Nishi K, Watts C, Reinheckel T, Schalkwijk J, Zeeuwen PL (2006) Cystatin M/E is a high affirmity inhibitor of cathepsin Vand cathepsin L by a reactive site that is distinct from the legumain binding site. A novel clue for the role of cystatin M/E in epidermal cornification. J Biol Chem 281:15893-15899
18. Cheng T, Tjabringa GS, Van Vlijmen-Willems IM, Hitomi K, Van Erp PE, Schalkwijk J, Zeeuwen PL (2009) The cystatin M/E controlled pathway of skin barrier formation: expression of its key components in psoriasis and atopic dermatitis. Br J Dermatol 161:253-264
19. Cornish-Bowden A (2002) Enthalpy-entropy compensation: a phantom phenomenon. J Biosci 27:121-126
20. Denecker G, Hoste E, Gilbert B, Hochepied T, Ovaere P, Lippens S (2007) Caspase-14 protects against epidermal UVB photo damage and water loss. Nat Cell Biol 9:666-674
21. Denecker G, Ovaere P, Petal V (2008) Caspase-14 reveals its secrets. J Cell Biol 180:451-458
22. Dennemärker J, Lohmüller T, Mayerle J, Tacke M, Lerch MM, Coussens LM, Peters C, Reinheckel T (2010) Deficiency for the cysteine protease cathepsin L promotes tumor progression in mouse epidermis. Oncogene 29:1611-1621
23. Devos M, Prawitt J, Staumont-Salle D, Hoste E, Fleury S, Bouchaert E, Gilbert B, Lippens S, Vandenabeele P, Dombrowicz D, Declercq W (2012) Filaggrin degradation by caspase-14 is required for UVB photoprotection but does not influence allergic sensitization in a mouse model of atopic dermatitis. J Invest Dermatol 132:2857-2860
24. Drenth J, Kalk KH, Swen HM (1976) Binding of chloromethyl ketone substrate analogues to crystalline papain. Biochemistry 15:3731-3738
25. Dunitz JD (1995) Win some lose some: enthalpy-entropy compensation in weak intermolecular interactions. Chem Biol 2:709-712
26. Eckhart L, Declercq W, Ban J, Rendl M, Lengauer B, Mayer C, Lippens S, Vandenabeele P, Tschachler E (2000) Terminal differentiation of human keratinocytes and stratum corneum formation is associated with caspase-14 activation. J Invest Dermatol 115:1148-1151
27. Eckhart L, Ballaun C, Uthman A, Kittel C, Stichenwirth M, Buchberger M, Fischer H, Sipos W, Tschachler E (2005) Identification and characterization of a novel mammalian caspase with proapoptotic activity. J Biol Chem 280:35077-35080
28. Fischer H, Stichenwirth M, Dockal M, Ghannadan M, Buchberger M, Bach J, Kapetanopoulos A, Declercq W, Tschachler E, Eckhart L (2004) Stratum corneum-derived caspase-14 is catalytically active. FEBS Lett 577:446-450
29. Galluzzi L, Vitale I, Abrams JM, Alnemri ES, Baehrecke EH, Blagosklonny MV, Dawson TM, Dawson VL, El-Deiry WS, Fulda S, Gottlieb E, Green DR, Hengartner MO, Kepp O, Knight RA, Kumar S, Lipton SA, Lu X, Madeo F, Malorni W, Mehlen P, Nuñez G, Peter ME, Piacentini M, Rubinsztein DC, Shi Y, Simon HU, Vandenabeele P, White E, Yuan J, Zhivotovsky B, Melino G, Kroemer G (2012) Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death. Cell Death Differ 19:107-120
30. Gul G, Mellor GW, Thomas EW, Brocklehurst K (2006) Temperature dependences of the kinetics of the reactions of papain and actinidin with a series of recovering probes differing in key molecular recognition features. Biochem J 396:17-21
31. Gul G, Hussain S, Thomas MP, Resmini M, Verma CS, Thomas EW, Brocklehurst K (2008) Generation of nucleophilic character in the Cys 25/His 159 ion-pair of papain involves Trp177 but not Asp158. Biochemistry 47:2025-2035
32. Hagemann S, Gunther T, Dennemarker J, Lohmuller T, Bromme D, Schule R (2004) The human cysteine protease cathepsin V can compensate for murine cathepsin L in mouse epidermis and hair follicles. Eur J Cell Biol 83:775-780
33. Hene IB, Mattis JA, Fruton JS (1979) Interaction of papain with derivatives of phenylalanylglycinal: fluorescence studies. Proc Natl Acad Sci USA 76:1131-1134
34. Hussain S, Khan A, Brocklehurst K (2002) A review of developments in the study of cysteine proteinase mechanism: opportunities for investigation of electrostatic effects and dynamic aspects of molecular recognition in enzyme chemistry. Recent Res Dev Biochem 3:653-677
35. Hussain S, Pinitglang S, Bailey TSF, Reid JD, Noble MA, Resmini M, Thomas EW, Greaves RB, Verma CS, Brocklehurst K (2003) Variation in the pH-dependent pre-steady-state and steady-state kinetic characteristics of cysteine-proteinase mechanism: evidence for electrostatic modulation of catalytic-site function by the neighbouring carboxylate anion. Biochem J 372:735-746
36. Hussain S, Khan A, Gul S, Resmini M, Verma CS, Thomas EW, Brocklehurst K (2011) Identification of interactions involved in the generation of nucleophilic reactivity and of catalytic competence in the catalytic site Cys/His ion-pair of papain. Biochemistry 50:10732-10742
37. Huber CP, Ozaki Y, Pliura DH, Storer AC, Carey PR (1982) Precise structural information for transient enzyme-substrate complexes by a combined X-ray crystallographic-resonance Raman spectroscopic approach. Biochemisrry 21:3109-3115
38. Kato T, Takai T, Mitsuishi K, Okumura K, Ogawa H (2005) Cystatin A inhibits IL-8 production by keratinocytes stimulated with Der p 1 and Der f 1: biochemical skin barrier against mite cysteine proteases. J Allergy Clin Immunol 116:169-176
39. Kazem S, Meijden E van der, Struijk L, Gruijl FR de, Feltkamp MC (2012) Human papillomavirus 8 E6 disrupts terminal skin differentiation and prevents pro-Caspase-14 cleavage. Virus Res 163:609-616
40. Koenig U, Eckhart L, Tschachler E (2001) Evidence that caspase-13 is not a human but a bovine gene. Biochem Biophys Res Commun 285:1150-1154
41. Kovalenko A, Kim JC, Kang TB, Rajput A, Bogdanov K, Dittrich-Breiholz O, Kracht M, Brenner O, Wallach D (2009) Caspase- 8 deficiency in epidermal keratinocytes triggers an inflammatory skin disease. J Exp Med 206:2161-2177
42. Kowlessur D, Topham CM, Thomas EW, O'Driscoll M, Templeton W, Brocklehurst K (1989) Identification of signalling and nonsignalling binding contributions to enzyme reactivity. Alternate contributions of binding interactions provide for change in transition state geometry in reaction of papain. Biochem J 258:755-764
43. Krug RR, Hunter WG, Greiger RA (1976a) Enthalpy-entropy compensation. 1. Some fundamental statistical problems associated with the analysis of Van't Hoff and Arrhenius data. J Phys Chem 80:2335-2340
44. Krug RR, Hunter WG, Greiger RA (1976b) Enthalpy-entropy compensation. 2. Separation of the chemical from the statistical effect. J Phys Chem 80:2341-2351
45. Lee P, Lee DJ, Chan C, Chen SW, Chen I, Jamora C (2009) Dynamic expression of epidermal caspase 8 simulates a wound healing response. Nature 458:519-523
46. Lippens S, Kockx M, Knaapen M, Mortier L, Polakowska R, Verheyen A, Garmyn M, Zwijsen A, Formstecher P, Huylebroeck D, Vandenabeele P, Declercq W (2000) Epidermal differentiation does not involve the pro-apoptotic executioner caspases, but is associated with caspase-14 induction and processing. Cell Death Differ 7:1218-1224
47. Lippens S, Kockx M, Denecker G, Knaapen M, Verheyen A, Christiaen R, Tschachler E, Vandenabeele P, Declercq W (2004) Vitamin D3 induces caspase-14 expression in psoriatic lesions and enhances caspase-14 processing in organotypic skin cultures. Am J Pathol 165:833-841
48. Lowe G (1976) The cysteine proteinases. Tetrahedron 32:291-302
49. Lowe G, Williams A (1965) Direct evidence for an acylated thiol as an intermediate in papain and ficincatalysed hydrolysis. Biochem J 96:189-193
50. Mellor GW, Thomas EW, Topham CM, Brocklehurst K (1993) The ionization characteristics of the Cys 25His 159 interactive system and of the modulatory group of papain. Resolution of ambiguity by electronic perturbation of the quasi-2-mercaptopyridine leaving group in a new pyrimidyl disulphide reactivity probe. Biochem J 290:75-83
51. Menard R, Carriere J, Laflamme P, Plouffe C, Khouri H, Vernet T, Tessier DC, Thomas DY, Storer AC (1991) Contribution of the glutamine 19 sidechain to transition state stabilization in the oxyarion hole of papain. Biochemistry 30:8924-8928
52. Menard R, Plouffe C, Laflamme P, Vernet T, Tessier DC, Thomas DY, Storer AC (1995) Modification of the electrostatic environment is tolerated in the oxyarion hole of the cysteine protease papain. Biochemistry 34:464-471
53. Mielgo A, Torres VA, Schmid MC, Graf R, Zeitlin SG, Lee P, Shields DJ, Barbero S, Jamora C, Stupack DG (2009) The death effector domains of caspase-8 induce terminal differentiation. PLoS One 4:e7879
54. Noble MA, Gul S, Verma CS, Brocklehurst K (2000) The ionization characteristics and chemical influences of aspartic acid residue 158 of papain and caricain determined by structure-related kinetic and computational techniques: multiple electrostatic modulators of active centre chemistry. Biochem J 351:723-733
55. Patel M, Kayani S, Templeton W, Mellor GW, Thomas EW, Brocklehurst K (1992) Evaluation of hydrogen bonding and enantiomeric P2-S2 hydrophobic contacts in dynamic aspects of molecular recognition by papain. Biochem J 287:881-889
56. Pinitglang S, Watts AB, Patel M, Reid JD, Noble MA, Gul S, Bokth A, Naeem A, Patel H, Thomas EW, Sreedharan S, Verma C, Brocklehurst K (1997) A classical enzyme active centre motif lacks catalytic competence until modulated electrostatically. Biochemistry 36:9968-9982
57. Raymond AA, Méchin MC, Nachat R, Toulza E, Tazi-Ahnini R, Serre G, Simon M (2007) Nine procaspases are expressed in normal human epidermis, but only caspase-14 is fully processed. Br J Dermatol 156:420-427
58. Reid JD, Hussain S, Sreedharan SK, Bailey TSF, Pinitglan S, Thomas EW, Verma CS, Brocklehurst K (2001) Variation in aspects of cysteine proteinase catalytic mechanism deduced spectroscopic observation of dithioester intermediates, kinetic analysis and molecular dynamics simulations. Biochem J 357:343-352
59. Reinheckel T, Hagemann S, Dollwet-Mack S, Martinez E, Lohmuller T, Zlatkovic G (2005) The lysosomal cysteine protease cathepsin L regulates keratinocyte proliferation by control of growth factor recycling. J Cell Sci 118:3387-3395
60. Roth W, Deussing J, Botchkarev VA, Pauly-Evers M, Saftig P, Hafner A (2000) Cathepsin L deficiency as molecular defect of furless: hyperproliferation of keratinocytes and pertubation of hair follicle cycling. FASEB J 14:2075-2086
61. Rubach JK, Cui G, Schneck JL, Taylor AN, Zhao B, Smallwood A, Nevins N, Wisnoski D, Thrall SH, Meek TD (2012) The aminoacid substituents of dipeptide substrates of cathepsin C can determine the rate-limiting steps of catalysis. Biochemistry (in press)
62. Samuelsson L, Stiller C, Friberg C, Nilsson C, Inerot A, Wahlström J (2004) Association analysis of cystatin A and zinc finger protein 148, two genes located at the psoriasis susceptibility locus PSORS5. J Invest Dermatol 122:1399-1400
63. Simpson RJ (2004) Purifying proteins for proteomics: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
64. Smith FJ, Irvine AD, Terron-Kwiatkowski A, Sandilands A, Campbell LE, Zhao Y (2006) Loss-of-function mutations in the gene encoding filaggrin cause ichthyosis vulgaris. Nat Genet 38:337-342
65. Steven AC, Steinert PM (1994) Protein composition of cornified cell envelopes of epidermal keratinocytes. J Cell Sci 107:693-700
66. Storer AC, Lee H, Carey PR (1983) Relaxed and perturbed substrate conformations in enzyme active sites: evidence from multichannel resonance Raman spectra. Biochemistry 22:4789-4796
67. Sundberg JP, Boggess D, Hogan ME, Sundberg BA, Rourk MH, Harris B (1997) Harlequin ichthyosis (ichq): a juvenile lethal mouse mutation with ichthyosiform dermatitis. Am J Pathol 151:293-310
68. Tholen S, Biniossek ML, Gansz M, Gomez-Auli A, Werner F, Noel A, Kizhakkedathu JN, Boerries M, Busch H, Reinheckel T, Schilling O (2012) Deletion of cysteine cathepsins B or L yields differential impacts on murine skin proteome and degradome. Mol Cell Proteomics (in press)
69. Turk V, Turk B, Turk D (2001) Lysosomal cysteine proteases: facts and opportunities. EMBO J 20:4629-4633
70. Van de Craen M, Vandenabeele P, Declercq W, Van den Brande I, Van Loo G, Molemans F, Schotte P, Van Criekinge W, Beyaert R, Fiers W (1997) Characterization of seven murine caspase family members. FEBS Lett 403:61-69
71. Vasilopoulos Y, Sagoo GS, Cork MJ, Walters K, Tazi-Ahnini R (2011) HLA-C, CSTA and DS12346 susceptibility alleles confer over 100-fold increased risk of developing psoriasis: evidence of gene interaction. J Hum Genet 56:423-427
72. Wu NL, Lee TA, Tsai TL, Lin WW (2011) TRAIL-induced keratinocyte differentiation requires caspase activation and p63 expression. J Invest Dermatol 131:874-883
73. Yuan J (2006) Divergence from a dedicated cellular suicide mechanism: exploring the evolution of cell death. Mol Cell 23:1-12
74. Zeeuwen PL, Vlijmen-Willems IM, Jansen BJ, Sotiropoulou G, Curfs JH, Meis JF (2001) Cystatin M/E expression is restricted to differentiated epidermal keratinocytes and sweat glands: a new skin-specific proteinase inhibitor that is a target for cross-linking by transglutaminase. J Invest Dermatol 116:693-701
75. Zeeuwen PL, Vlijmen-Willems IM, Hendriks W (2002) A null mutation in the cystatin M/E gene of ichq mice causes juvenile lethality and defects in epidermal cornification. Hum Mol Genet 11:2867-2875
76. Zeeuwen PL, Dale BA, De Jongh G, Vlijmen-Willems IM, Fleckman P, Kimball JR (2003) The human cystatin M/E gene (CST6): exclusion as a candidate gene for harlequin ichthyosis. Invest Dermatol 121:65-68
77. Zeeuwen PL, Van Vlijmen-Willems IM, Olthuis D, Johansen HT, Hitomi K, Hara-Nishimura I, Powers JC, James KE, Camp HJ op den, Lemmens R, Schalkwijk J (2004) Evidence that unrestricted legumain activity is involved in disturbed epidermal cornification in cystatin M/E deficient mice. Hum Mol Genet 13:1069-1079
78. Zeeuwen PLJM, Ishida-Yamamoto A, Van Vlijmen-Willems IMJJ, Cheng T, Berges M, Iizuka H, Schalwijk J (2007) Colocalization of cystatin M/E and cathepsin V in lamellar granules and corneodesmosomes suggests a functional role in epidermal differentiation. J Invest Dermatol 127:120-128
79. Zeeuwen PL, Cheng T, Schalwijk J (2009) The biology of cystatin M/E and its cognate target protease. J Invest Dermatol 129:1327-1338
80. Zeeuwen PL, Van Vlijmen-Willems IM, Cheng T, Rodijk-Olthuis D, Hitomi K, Hara-Nishimura I, John S, Smyth N, Reinheckel T, Hendriks WJ, Schalkwijk J (2010) The cystatin M/E-cathepsin L balance is essential for tissue homeostasis in epidermis, hair follicles, and cornea. FASEB J 24:3744-3755