Advertisement

Stability of Therapeutic Enzymes: Challenges and Recent Advances

  • Shubhrima Ghosh
  • Shahenvaz Alam
  • Anurag S. Rathore
  • S. K. KhareEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1148)

Abstract

Enzymes are biocatalysts that have found profound applications in the current biotherapeutic industry and play a crucial role in diagnosis, prevention, and biochemical analysis of major diseases. However, stability, protein degradation and immunogenicity in the body present unique challenges that are faced upon sustained use of such enzymes. The present chapter is an attempt to dissect the state-of-the-art in relation to the challenges of development of therapeutic enzymes and the recent advances to address them. At the very outset, diseases where enzymes have found effective applications and the various causes of enzyme instability have been discussed. In recent times, polymer or nano- conjugated resistant delivery methods, as well as mutagenesis have led to manifold increase in enzyme stability against thermal denaturation, acidic gut environment, proteolysis and immunogenicity. Further, methods of analytical characterization of proteins have been highlighted and explored to shape future research directions.

Keywords

Enzyme Metabolic disorders Immunogenicity Protein denaturation Mutagenesis 

Abbreviations

US

United States

FDA

Food and drug administration

AML

Acute Myeloid Leukemia

ALL

Acute Lymphoblastic Leukemia

PEG

Polyethylene glycol

ADP

Adenosine Diphosphate

NAD

Nicotinamide Adenine Dinucleotide

ERT

Enzyme Replacement Therapy

GAG

Glucosaminoglycans

DNA

Deoxyribonucleic Acid

LAL

Lysosomal Acid Lipase

MPS

Mucopolysaccharidosis

LIPA

Lysosomal Acid Lipase

SCID

Severe Combined Immune Deficiency

ADA

Adenosine Deaminase

PPFE

Pleuroparenchymal Fibroelastosis

RNA

Ribonucleic Acid

DUB

Deubiquitinating Enzyme

GI

Gastrointestinal

BAb

Binding Antibodies

GD

Gaucher’s Disease

GALK1

Galactokinase 1

EC

Enzyme Commission

ATP

Adenosine Triphosphate

ABD

Albumin-Binding Domain

PVP

Poly(N-vinylpyrrolidone)

LbL

Layer-by-layer

MNP

Magnetic Nanoparticles

PAGE

Poly-Acrylamide Gel Electrophoresis

SDS

Sodium Dodecyl Sulfate

IEF

Isoelectric Focusing

2D

2-dimension

DIGE

Difference Gel Electrophoresis

HPLC

High-performance liquid chromatography

CD

Circular Dichroism

NMR

Nuclear Magnetic Resonance

XRD

X-ray Diffraction

FTIR

Fourier-Transform Infrared Spectroscopy

IR

Infrared

DLS

Dynamic Light Scattering

HT-DLS

High- Throughput Dynamic Light Scattering

UVRR

Ultraviolet Resonance Raman

ROA

Raman Optical Activity

ANS

8-Anilinonaphthalene-1-sulfonic acid

ThT

Thioflavin-T

TEM

Transmission Electron Microscopy

ELISA

Enzyme-Linked Immunosorbent Assay

SPR

Surface Plasmon Resonance

BLI

Bio-Layer Interferometry

ITC

Isothermal Titration Calorimetry

tPa

Tissue Plasminogen Activator

SKA

Streptokinase

References

  1. Akash MSH, Rehman K, Tariq M, Chen S (2015) Development of therapeutic proteins: advances and challenges. Turk J Biol 39(3):343–358CrossRefGoogle Scholar
  2. Alain K, Querellou J (2009) Cultivating the uncultured: limits, advances and future challenges. Extremophiles 13(4):583–594PubMedCrossRefPubMedCentralGoogle Scholar
  3. Alegra T, Vairo F, de Souza MV, Krug BRC, Schwartz IVD (2012) Enzyme replacement therapy for Fabry disease: a systematic review and meta-analysis. Genet Mol Biol 35(4):947–954PubMedPubMedCentralCrossRefGoogle Scholar
  4. Alpers D (2008) Role of lipoprotein lipase in triglyceride metabolism: potential therapeutic target. Futur Lipidol 3(4):385–397CrossRefGoogle Scholar
  5. Anderson VL, Webb WW (2011) Transmission electron microscopy characterization of fluorescently labelled amyloid β 1-40 and α-synuclein aggregates. BMC Biotechnol 11(1):125PubMedPubMedCentralCrossRefGoogle Scholar
  6. Angelini C, Semplicini C (2012) Enzyme replacement therapy for Pompe disease. Curr Neurol Neurosci Rep 12(1):70–75PubMedCrossRefPubMedCentralGoogle Scholar
  7. Baker EN, Hubbard RE (1984) Hydrogen bonding in globular proteins. Prog Biophys Mol Biol 44(2):97–179PubMedCrossRefPubMedCentralGoogle Scholar
  8. Bakshi RP, Shapiro TA (2003) DNA topoisomerases as targets for antiprotozoal therapy. Mini-Rev Med Chem 3(6):597–608PubMedCrossRefPubMedCentralGoogle Scholar
  9. Balci H, Ozturk MT, Pijning T, Ozturk SI, Gumusel F (2014) Improved activity and pH stability of E. coli ATCC 11105 penicillin acylase by error-prone PCR. Appl Microbiol Biotechnol 98(10):4467–4477PubMedCrossRefPubMedCentralGoogle Scholar
  10. Berkowitz SA (2017) Analytical characterization: structural assessment of biosimilarity. In: Biosimilar drug product development. CRC Press, Boca Raton, pp 15–82CrossRefGoogle Scholar
  11. Bui LA, Hurst S, Finch GL, Ingram B, Jacobs IA, Kirchhoff CF, Ng CK, Ryan AM (2015) Key considerations in the preclinical development of biosimilars. Drug Discov Today 20:3–15PubMedCrossRefPubMedCentralGoogle Scholar
  12. Burley SK, Petsko GA (1988) Weakly polar interactions in proteins. In: Advances in protein chemistry. Elsevier, New York, pp 125–189Google Scholar
  13. But WM, Wong MY, Chow JC, Chan WKY, Ko WT, Wu SP, Wong ML, Miu TY, Tse WY, Hung WWY (2011) Enzyme replacement therapy for mucopolysaccharidosis VI (Maroteaux-Lamy syndrome): experience in Hong Kong. Hong Kong Med J 17(4):317–324PubMedPubMedCentralGoogle Scholar
  14. Calvo-Lerma J, Martínez-Barona S, Masip E, Fornés V, Ribes-Koninckx C (2017) Pancreatic enzyme replacement therapy in cystic fibrosis: dose, variability and coefficient of fat absorption. Rev Esp Enferm Dig Organo Oficial Soc Esp Patol Dig 109(10):684–689Google Scholar
  15. Cavalli A, Salvatella X, Dobson CM, Vendruscolo M (2007) Protein structure determination from NMR chemical shifts. Proc Natl Acad Sci 104(23):9615–9620PubMedCrossRefPubMedCentralGoogle Scholar
  16. Chabot JA, Tsai WY, Fine RL, Chen C, Kumah CK, Antman KA, Grann VR (2010) Pancreatic proteolytic enzyme therapy compared with gemcitabine-based chemotherapy for the treatment of pancreatic cancer. J Clin Oncol 28(12):2058PubMedCrossRefPubMedCentralGoogle Scholar
  17. Chan B, Wara D, Bastian J, Hershfield MS, Bohnsack J, Azen CG, Parkman R, Weinberg K, Kohn DB (2005) Long-term efficacy of enzyme replacement therapy for adenosine deaminase (ADA)-deficient severe combined immunodeficiency (SCID). Clin Immunol 117(2):133–143PubMedCrossRefPubMedCentralGoogle Scholar
  18. Chibale K (2002) Towards broadspectrum antiprotozoal agents. Arkivoc 9:93–98Google Scholar
  19. Chorny M, Hood E, Levy RJ, Muzykantov VR (2010) Endothelial delivery of antioxidant enzymes loaded into non-polymeric magnetic nanoparticles. J Control Release 146(1):144–151PubMedPubMedCentralCrossRefGoogle Scholar
  20. Choudhary B, Nagpure A, Gupta RK (2014) Fungal cell-wall lytic enzymes, antifungal metabolite (s) production, and characterization from Streptomyces exfoliatus MT9 for controlling fruit-rotting fungi. J Basic Microbiol 54(12):1295–1309PubMedCrossRefPubMedCentralGoogle Scholar
  21. Chuang HY, Suen CS, Hwang MJ, Roffler SR (2015) Toward reducing immunogenicity of enzyme replacement therapy: altering the specificity of human β-glucuronidase to compensate for α-iduronidase deficiency. Protein Eng Des Sel 28(11):519–530PubMedCrossRefPubMedCentralGoogle Scholar
  22. Cocci A, Russo GI, Briganti A, Salonia A, Cacciamani G, Capece M, Falcone M, Timpano M, Cito G, Verze P (2018) Predictors of treatment success after collagenase clostridium histolyticum injection for Peyronie’s disease. Development of a nomogram from a multicentre single-arm, non-placebo controlled clinical study. BJU Int 122:680–687PubMedCrossRefPubMedCentralGoogle Scholar
  23. Cook MT, Tzortzis G, Charalampopoulos D, Khutoryanskiy VV (2012) Microencapsulation of probiotics for gastrointestinal delivery. J Control Release 162(1):56–67PubMedCrossRefPubMedCentralGoogle Scholar
  24. Da Silva EM, Strufaldi MW, Andriolo RB, Silva LA (2011) Enzyme replacement therapy with idursulfase for mucopolysaccharidosis type II (Hunter syndrome). Cochrane Database Syst Rev 11(11)Google Scholar
  25. DeLong RK, Reynolds CM, Malcolm Y, Schaeffer A, Severs T, Wanekaya A (2010) Functionalized gold nanoparticles for the binding, stabilization, and delivery of therapeutic DNA, RNA, and other biological macromolecules. Nanotechnol Sci Appl 3:53PubMedPubMedCentralCrossRefGoogle Scholar
  26. Desai UR (2004) New antithrombin-based anticoagulants. Med Res Rev 24(2):151–181PubMedCrossRefPubMedCentralGoogle Scholar
  27. Doig AJ, Williams DH (1991) Is the hydrophobic effect stabilizing or destabilizing in proteins?: The contribution of disulphide bonds to protein stability. J Mol Biol 217(2):389–398PubMedCrossRefPubMedCentralGoogle Scholar
  28. Duval M, Suciu S, Ferster A, Rialland X, Nelken B, Lutz P, Benoit Y, Robert A, Manel A-M, Vilmer E (2002) Comparison of Escherichia coli-asparaginase with Erwinia-asparaginase in the treatment of childhood lymphoid malignancies: results of a randomized European Organisation for Research and Treatment of Cancer-Children’s Leukemia Group phase 3 trial. Blood 99(8):2734–2739PubMedCrossRefPubMedCentralGoogle Scholar
  29. Dziubla TD, Karim A, Muzykantov VR (2005) Polymer nanocarriers protecting active enzyme cargo against proteolysis. J Control Release 102(2):427–439PubMedCrossRefPubMedCentralGoogle Scholar
  30. Egler RA, Ahuja SP, Matloub Y (2016) L-asparaginase in the treatment of patients with acute lymphoblastic leukemia. J Pharmacol Pharmacother 7(2):62PubMedPubMedCentralCrossRefGoogle Scholar
  31. Ehren J, Govindarajan S, Morón B, Minshull J, Khosla C (2008) Protein engineering of improved prolyl endopeptidases for celiac sprue therapy. Protein Eng Des Sel 21(12):699–707PubMedPubMedCentralCrossRefGoogle Scholar
  32. Fekete S, Guillarme D, Sandra P, Sandra K (2015) Chromatographic, electrophoretic, and mass spectrometric methods for the analytical characterization of protein biopharmaceuticals. Anal Chem 88(1):480–507PubMedCrossRefPubMedCentralGoogle Scholar
  33. Fuhrmann G, Leroux JC (2011) In vivo fluorescence imaging of exogenous enzyme activity in the gastrointestinal tract. Proc Natl Acad Sci 108(22):9032–9037PubMedCrossRefPubMedCentralGoogle Scholar
  34. Fuhrmann G, Leroux JC (2014) Improving the stability and activity of oral therapeutic enzymes-recent advances and perspectives. Pharm Res 31(5):1099–1105PubMedCrossRefPubMedCentralGoogle Scholar
  35. Gámez A, Wang L, Straub M, Patch MG, Stevens RC (2004) Toward PKU enzyme replacement therapy: PEGylation with activity retention for three forms of recombinant phenylalanine hydroxylase. Mol Ther 9(1):124–129PubMedCrossRefPubMedCentralGoogle Scholar
  36. Ghaffarinia A, Jalili C, Riazi-Rad F, Mostafaie A, Parvaneh S, Pakravan N (2014) Anti-inflammatory effect of chymotrypsin to autoimmune response against CNS is dose-dependent. Cell Immunol 292(1–2):102–108PubMedCrossRefPubMedCentralGoogle Scholar
  37. Ghosh P, Han G, De M, Kim CK, Rotello VM (2008) Gold nanoparticles in delivery applications. Adv Drug Deliv Rev 60(11):1307–1315PubMedCrossRefPubMedCentralGoogle Scholar
  38. Ghosh S, Tiwari R, Hemamalini R, Khare SK (2017) Multi-omic approaches for mapping interactions among marine microbiomes. In: Understanding host-microbiome interactions-an omics approach. Springer, pp 353–368Google Scholar
  39. Ghosh S, Ahmad R, Gautam VK, Khare SK (2018) Cholesterol-oxidase-magnetic nanobioconjugates for the production of 4-cholesten-3-one and 4-cholesten-3, 7-dione. Bioresour Technol 254:91–96PubMedCrossRefPubMedCentralGoogle Scholar
  40. Gökmen V (2015) Acrylamide in food: analysis, content and potential health effects. Academic, AmsterdamGoogle Scholar
  41. Goodsell DS (2005) The molecular perspective: L-asparaginase. Oncologist 10(3):238–239PubMedCrossRefPubMedCentralGoogle Scholar
  42. Greenfield NJ (2006) Using circular dichroism spectra to estimate protein secondary structure. Nat Protoc 1(6):2876PubMedPubMedCentralCrossRefGoogle Scholar
  43. Griswold KE, Bement JL, Teneback CC, Scanlon TC, Wargo MJ, Leclair LW (2014) Bioengineered lysozyme in combination therapies for Pseudomonas aeruginosa lung infections. Bioengineered 5(2):143–147PubMedPubMedCentralCrossRefGoogle Scholar
  44. Hamuro Y, Coales SJ, Molnar KS, Tuske SJ, Morrow JA (2008) Specificity of immobilized porcine pepsin in H/D exchange compatible conditions. Rapid Commun Mass Spectrom 22(7):1041–1046PubMedCrossRefPubMedCentralGoogle Scholar
  45. Harmatz P (2015) Enzyme replacement therapies and immunogenicity in lysosomal storage diseases: is there a pattern? Clin Ther 37(9):2130–2134PubMedCrossRefPubMedCentralGoogle Scholar
  46. Harris JM, Chess RB (2003) Effect of pegylation on pharmaceuticals. Nat Rev Drug Discov 2(3):214PubMedCrossRefPubMedCentralGoogle Scholar
  47. Haxho F, Neufeld RJ, Szewczuk MR (2016) Neuraminidase-1: a novel therapeutic target in multistage tumorigenesis. Oncotarget 7(26):40860PubMedPubMedCentralCrossRefGoogle Scholar
  48. Hayashi S, Yokoyama I, Namii Y, Emi N, Uchida K, Takagi H (1999) Inhibitory effect on the establishment of hepatic metastasis by transduction of the tissue plasminogen activator gene to murine colon cancer. Cancer Gene Ther 6(4):380PubMedCrossRefPubMedCentralGoogle Scholar
  49. Hendsch ZS, Tidor B (1994) Do salt bridges stabilize proteins? A continuum electrostatic analysis. Protein Sci 3(2):211–226PubMedPubMedCentralCrossRefGoogle Scholar
  50. Hershfield MS, Chaffee S, Sorensen RU (1993) Enzyme replacement therapy with polyethylene glycol-adenosine deaminase in adenosine deaminase deficiency: overview and case reports of three patients, including two now receiving gene therapy. Pediatr Res 33(S4):S42PubMedCrossRefPubMedCentralGoogle Scholar
  51. Huynen C, Filée P, Matagne A, Galleni M, Dumoulin M (2013) Class a-lactamases as versatile scaffolds to create hybrid enzymes: applications from basic research to medicine. Biomed Res Int 2013:1–6CrossRefGoogle Scholar
  52. Ilinskaya ON, Mahmud RS (2014) Ribonucleases as antiviral agents. Mol Biol 48(5):615–623CrossRefGoogle Scholar
  53. Illanes A, Valencia P (2017) Industrial and therapeutic enzymes: penicillin acylase. In: Current developments in biotechnology and bioengineering. Elsevier, Amsterdam, pp 267–305CrossRefGoogle Scholar
  54. Imrie CW, Connett G, Hall RI, Charnley RM (2010) Enzyme supplementation in cystic fibrosis, chronic pancreatitis, pancreatic and periampullary cancer. Aliment Pharmacol Ther 32:1–25PubMedCrossRefPubMedCentralGoogle Scholar
  55. Ishihara T, Tanaka KI, Tasaka Y, Namba T, Suzuki J, Ishihara T, Okamoto S, Hibi T, Takenaga M, Igarashi R (2009) Therapeutic effect of lecithinized superoxide dismutase against colitis. J Pharmacol Exp Ther 328(1):152–164PubMedCrossRefPubMedCentralGoogle Scholar
  56. Jayachandran S, Khobre P (2017) Efficacy of bromelain along with trypsin, rutoside trihydrate enzymes and diclofenac sodium combination therapy for the treatment of TMJ osteoarthritis-a randomised clinical trial. J Clin Diagn Res 11(6):ZC09PubMedPubMedCentralGoogle Scholar
  57. Kaminetzky D, Hymes KB (2008) Denileukin diftitox for the treatment of cutaneous T-cell lymphoma. Biol Targets Ther 2(4):717Google Scholar
  58. Karamitros CS, Yashchenok AM, Möhwald H, Skirtach AG, Konrad M (2013) Preserving catalytic activity and enhancing biochemical stability of the therapeutic enzyme asparaginase by biocompatible multilayered polyelectrolyte microcapsules. Biomacromolecules 14(12):4398–4406PubMedCrossRefPubMedCentralGoogle Scholar
  59. Karstad R, Isaksen G, Wynendaele E, Guttormsen Y, De Spiegeleer B, Brandsdal BO, Svendsen JS, Svenson J (2012) Targeting the S1 and S3 subsite of trypsin with unnatural cationic amino acids generates antimicrobial peptides with potential for oral administration. J Med Chem 55(14):6294–6305PubMedCrossRefPubMedCentralGoogle Scholar
  60. Kasturi L, Amin Alpa S (2001) Enzyme replacement therapy in Gaucher’s disease. Indian Pediatr 38(6):686–687PubMedPubMedCentralGoogle Scholar
  61. Kini RM (2005) Structure-function relationships and mechanism of anticoagulant phospholipase A2 enzymes from snake venoms. Toxicon 45(8):1147–1161PubMedCrossRefPubMedCentralGoogle Scholar
  62. Kishimoto TK, Ferrari JD, LaMothe RA, Kolte PN, Griset AP, O'Neil C, Chan V, Browning E, Chalishazar A, Kuhlman W (2016) Improving the efficacy and safety of biologic drugs with tolerogenic nanoparticles. Nat Nanotechnol 11(10):890PubMedCrossRefPubMedCentralGoogle Scholar
  63. Knappe D, Goldbach T, Hatfield MPD, Palermo NY, Weinert S, Sträter N, Hoffmann R, Lovas SN (2016) Proline-rich antimicrobial peptides optimized for binding to Escherichia coli chaperone DnaK. Protein Pept Lett 23(12):1061–1071PubMedCrossRefPubMedCentralGoogle Scholar
  64. Kong J, Yu S (2007) Fourier transform infrared spectroscopic analysis of protein secondary structures. Acta Biochim Biophys Sin 39(8):549–559CrossRefPubMedGoogle Scholar
  65. Kosky AA, Razzaq UO, Treuheit MJ, Brems DN (1999) The effects of alpha-helix on the stability of Asn residues: deamidation rates in peptides of varying helicity. Protein Sci 8(11):2519–2523PubMedPubMedCentralCrossRefGoogle Scholar
  66. Krizsan A, Volke D, Weinert S, Sträter N, Knappe D, Hoffmann R (2014) Insect-derived proline-rich antimicrobial peptides kill bacteria by inhibiting bacterial protein translation at the 70 S ribosome. Angew Chem Int Ed 53(45):12236–12239CrossRefGoogle Scholar
  67. Lamppa JW, Griswold KE (2013) Alginate lyase exhibits catalysis-independent biofilm dispersion and antibiotic synergy. Antimicrob Agents Chemother 57(1):137–145PubMedPubMedCentralCrossRefGoogle Scholar
  68. Langer V, Bhandari PS, Rajagopalan S, Mukherjee MK (2013) Enzymatic debridement of large burn wounds with papain-urea: is it safe? Med J Armed Forces India 69(2):144–150PubMedCrossRefPubMedCentralGoogle Scholar
  69. Lansigan F, Stearns DM, Foss F (2010) Role of denileukin diftitox in the treatment of persistent or recurrent cutaneous T-cell lymphoma. Cancer Manag Res 2:53PubMedPubMedCentralCrossRefGoogle Scholar
  70. Lee HR, Kim MI, Hong SE, Choi J, Kim YM, Yoon KR, Lee S, Ha SH (2016) Effect of functional group on activity and stability of lipase immobilized on silica-coated magnetite nanoparticles with different functional group. Anal Sci Technol 29(3):105–113CrossRefGoogle Scholar
  71. Leland PA, Raines RT (2001) Cancer chemotherapy-ribonucleases to the rescue. Chem Biol 8(5):405–413PubMedPubMedCentralCrossRefGoogle Scholar
  72. Li YM, Vallera DA, Hall WA (2013) Diphtheria toxin-based targeted toxin therapy for brain tumors. J Neuro-Oncol 114(2):155–164CrossRefGoogle Scholar
  73. Liao AY, Ghosh A, O’Leary C, Mercer J, Church HJ, Tylee KL, Goenka A, Holley R, Wynn RF, Jones SA (2018) Induction of immune tolerance to enzyme replacement therapy in mucopolysaccharidosis type I. Mol Genet Metab 123(2):S86CrossRefGoogle Scholar
  74. Lindgren J, Eriksson Karlström A (2014) Intramolecular thioether crosslinking of therapeutic proteins to increase proteolytic stability. ChemBioChem 15(14):2132–2138PubMedCrossRefPubMedCentralGoogle Scholar
  75. Lu F, Lu Z, Bie X, Yao Z, Wang Y, Lu Y, Guo Y (2010) Purification and characterization of a novel anticoagulant and fibrinolytic enzyme produced by endophytic bacterium Paenibacillus polymyxa EJS-3. Thromb Res 126(5):e349–e355PubMedCrossRefPubMedCentralGoogle Scholar
  76. Luo Q, Joubert MK, Stevenson R, Ketchem RR, Narhi LO, Wypych J (2011) Chemical modifications in therapeutic protein aggregates generated under different stress conditions. J Biol Chem 286(28):25134–25144PubMedPubMedCentralCrossRefGoogle Scholar
  77. Lyseng-Williamson KA (2014) Elosulfase Alfa: a review of its use in patients with mucopolysaccharidosis type IVA (Morquio A syndrome). BioDrugs 28(5):465–475PubMedCrossRefPubMedCentralGoogle Scholar
  78. Mali N, Wavikar P, Vavia P (2015) Serratiopeptidase loaded chitosan nanoparticles by polyelectrolyte complexation: in vitro and in vivo evaluation. AAPS PharmSciTech 16(1):59–66PubMedCrossRefPubMedCentralGoogle Scholar
  79. Matuszewska A, Karp M, Jaszek M, Janusz G, Osińska-Jaroszuk M, Sulej J, Stefaniuk D, Tomczak W, Giannopoulos K (2016) Laccase purified from Cerrena unicolor exerts antitumor activity against leukemic cells. Oncol Lett 11(3):2009–2018PubMedPubMedCentralCrossRefGoogle Scholar
  80. McAuley M, Mesa-Torres N, McFall A, Morris S, Huang M, Pey A, Timson DJ (2018) Improving the activity and stability of human galactokinase for therapeutic and biotechnological applications. ChemBioChem 19:1088–1095PubMedCrossRefPubMedCentralGoogle Scholar
  81. McDonald IK, Thornton JM (1994) Satisfying hydrogen bonding potential in proteins. J Mol Biol 238(5):777–793PubMedCrossRefPubMedCentralGoogle Scholar
  82. Mitulović G, Mechtler K (2006) HPLC techniques for proteomics analysis-a short overview of latest developments. Brief Funct Genomics 5(4):249–260CrossRefGoogle Scholar
  83. Mohan Kumar NS, Kishore V, Manonmani HK (2014) Chemical modification of L-asparaginase from Cladosporium sp. for improved activity and thermal stability. Prep Biochem Biotechnol 44(5):433–450PubMedCrossRefPubMedCentralGoogle Scholar
  84. Mouneshkumar Chappi D, Suresh KV, Patil MR, Desai R, Tauro DP, Shiva Bharani KNS, Parkar MI, Babaji HV (2015) Comparison of clinical efficacy of methylprednisolone and serratiopeptidase for reduction of postoperative sequelae after lower third molar surgery. J Clin Exp Dent 7(2):e197CrossRefGoogle Scholar
  85. Muenzer J, Wraith JE, Beck M, Giugliani R, Harmatz P, Eng CM, Vellodi A, Martin R, Ramaswami U, Gucsavas-Calikoglu M (2006) A phase II/III clinical study of enzyme replacement therapy with idursulfase in mucopolysaccharidosis II (Hunter syndrome). Genet Med 8(8):465PubMedCrossRefPubMedCentralGoogle Scholar
  86. Nanduri B, Suvarnapunya AE, Venkatesan M, Edelmann MJ (2013) Deubiquitinating enzymes as promising drug targets for infectious diseases. Curr Pharm Des 19(18):3234–3247PubMedPubMedCentralCrossRefGoogle Scholar
  87. Nebija D, Noe CR, Urban E, Lachmann B (2014) Quality control and stability studies with the monoclonal antibody, trastuzumab: application of 1D-vs. 2D-gel electrophoresis. Int J Mol Sci 15(4):6399–6411PubMedPubMedCentralCrossRefGoogle Scholar
  88. Neurath H (1984) Evolution of proteolytic enzymes. Science 224(4647):350–357CrossRefGoogle Scholar
  89. Ngu LH, Peitee WO, Leong HY, Chew HB (2017) Case report of treatment experience with idursulfase beta (Hunterase) in an adolescent patient with MPS II. Mol Genet Metab Rep 12:28–32PubMedPubMedCentralCrossRefGoogle Scholar
  90. Nukolova NV, Aleksashkin AD, Abakumova TO, Morozova AY, Gubskiy IL, Kirzhanova EA, Abakumov MA, Chekhonin VP, Klyachko NL, Kabanov AV (2018) Multilayer polyion complex nanoformulations of superoxide dismutase 1 for acute spinal cord injury. J Control Release 270:226–236PubMedCrossRefPubMedCentralGoogle Scholar
  91. Nupur N, Chhabra N, Dash R, Rathore AS (2018) Assessment of structural and functional similarity of biosimilar products: rituximab as a case study. Translated by Taylor & Francis, pp 143–158Google Scholar
  92. Pattnaik P (2005) Surface plasmon resonance. Appl Biochem Biotechnol 126(2):79–92PubMedCrossRefPubMedCentralGoogle Scholar
  93. Perchellet EM, Wang Y, Weber RL, Lou K, Hua DH, Perchellet JPH (2004) Antitumor triptycene bisquinones induce a caspase-independent release of mitochondrial cytochrome c and a caspase-2-mediated activation of initiator caspase-8 and-9 in HL-60 cells by a mechanism which does not involve Fas signaling. Anti-Cancer Drugs 15(10):929–946PubMedCrossRefPubMedCentralGoogle Scholar
  94. Pierce MM, Raman CS, Nall BT (1999) Isothermal titration calorimetry of protein-protein interactions. Methods 19(2):213–221PubMedCrossRefPubMedCentralGoogle Scholar
  95. Pundir CS, Narang J, Chauhan N, Sharma P, Sharma R (2012) An amperometric cholesterol biosensor based on epoxy resin membrane bound cholesterol oxidase. Indian J Med Res 136(4):633PubMedPubMedCentralGoogle Scholar
  96. Qi Y, Chilkoti A (2015) Protein-polymer conjugation-moving beyond PEGylation. Curr Opin Chem Biol 28:181–193PubMedPubMedCentralCrossRefGoogle Scholar
  97. Ramirez Peña E, Treviño J, Liu Z, Perez N, Sumby P (2010) The group A Streptococcus small regulatory RNA FasX enhances streptokinase activity by increasing the stability of the ska mRNA transcript. Mol Microbiol 78(6):1332–1347PubMedPubMedCentralCrossRefGoogle Scholar
  98. Rathore AS (2009) Follow-on protein products: scientific issues, developments and challenges. Trends Biotechnol 27(12):698–705PubMedCrossRefPubMedCentralGoogle Scholar
  99. Reed GL, Liu L, Houng AK, Matsueda LH, Lizbeth H (1998) Mechanisms of fibrin-independent and fibrin-dependent plasminogen activation by streptokinase. Circulation 98(17):41–41Google Scholar
  100. Reichel C, Thevis M (2013) Gel electrophoretic methods for the analysis of biosimilar pharmaceuticals using the example of recombinant erythropoietin. Bioanalysis 5(5):587–602PubMedCrossRefPubMedCentralGoogle Scholar
  101. Rosenberg M, Kingma W, Fitzpatrick MA, Richards SM (1999) Immunosurveillance of alglucerase enzyme therapy for Gaucher patients: induction of humoral tolerance in seroconverted patients after repeat administration. Blood 93(6):2081–2088PubMedPubMedCentralGoogle Scholar
  102. Rosenberg L, Lapid O, Bogdanov-Berezovsky A, Glesinger R, Krieger Y, Silberstein E, Sagi A, Judkins K, Singer AJ (2004) Safety and efficacy of a proteolytic enzyme for enzymatic burn debridement: a preliminary report. Burns 30(8):843–850PubMedCrossRefPubMedCentralGoogle Scholar
  103. Sabu A (2003) Sources, properties and applications of microbial therapeutic enzymes. Indian J Biotechnol 2(2003):334–341Google Scholar
  104. Sarada KV (2013) Production and applications of L-glutaminase using fermentation technology. Asia Pac J Res 1:1Google Scholar
  105. Saunders SE, Bartz JC, Vercauteren KC, Bartelt-Hunt SL (2011) An enzymatic treatment of soil-bound prions effectively inhibits replication. Appl Environ Microbiol 77(13):4313–4317PubMedPubMedCentralCrossRefGoogle Scholar
  106. Sawhney P, Kumar S, Maheshwari N, Singh Guleria S, Dhar N, Kashyap R, Sahni G (2016) Site-specific thiol-mediated PEGylation of streptokinase leads to improved properties with clinical potential. Curr Pharm Des 22(38):5868–5878PubMedCrossRefPubMedCentralGoogle Scholar
  107. Scagnolari C, Bellomi F, Turriziani O, Bagnato F, Tomassini V, Lavolpe V, Ruggieri M, Bruschi F, Meucci G, Dicuonzo G (2002) Neutralizing and binding antibodies to IFN-β: relative frequency in relapsing-remitting multiple sclerosis patients treated with different IFN-β preparations. J Interf Cytokine Res 22(2):207–213CrossRefGoogle Scholar
  108. Schöneich C (2000) Mechanisms of metal-catalyzed oxidation of histidine to 2-oxo-histidine in peptides and proteins. J Pharm Biomed Anal 21(6):1093–1097PubMedCrossRefPubMedCentralGoogle Scholar
  109. Shah Mahmud R, Müller C, Romanova Y, Mostafa A, Ulyanova V, Pleschka S, Ilinskaya O (2017) Ribonuclease from Bacillus acts as an antiviral agent against negative-and positive-sense single stranded human respiratory RNA viruses. BioMed Res Int 2017Google Scholar
  110. Shahaboddin ME, Khajeh K, Maleki M, Golestani A (2017) Improvement of activity and stability of chondroitinase ABC I by introducing an aromatic cluster at the surface of protein. Enzym Microb Technol 105:38–44CrossRefGoogle Scholar
  111. Shak S, Capon DJ, Hellmiss R, Marsters SA, Baker CL (1990) Recombinant human DNase I reduces the viscosity of cystic fibrosis sputum. Proc Natl Acad Sci 87(23):9188–9192PubMedCrossRefPubMedCentralGoogle Scholar
  112. Shaked ZE, Wolfe S (1988) Stabilization of pyranose 2-oxidase and catalase by chemical modification. In: Methods in enzymology, pp 599–615Google Scholar
  113. Shlyakhovenko VO (2016) Ribonucleases. Possible new approach in cancer therapy. Exp Oncol 38(1):2–8PubMedCrossRefPubMedCentralGoogle Scholar
  114. Sikri N, Bardia A (2007) A history of streptokinase use in acute myocardial infarction. Tex Heart Inst J 34(3):318PubMedPubMedCentralGoogle Scholar
  115. Some D, Burge R (2015) Innovations in automation-high-throughput dynamic light scattering for screening biotherapeutic formulations. Biopharm Int 28(11):23Google Scholar
  116. Su K, Donaldson E, Sharma R (2016) Novel treatment options for lysosomal acid lipase deficiency: critical appraisal of sebelipase alfa. Appl Clin Genet 9:157PubMedPubMedCentralCrossRefGoogle Scholar
  117. Tanford C (1980) The hydrophobic effect: formation of micelles and biological membranes, 2nd edn. Wiley, BrisbaneGoogle Scholar
  118. Tatsumoto KM, Oh KK, Baker JO, Himmel ME (1989) Enhanced stability of glucoamylase through chemical crosslinking. Appl Biochem Biotechnol 20(1):293–308CrossRefGoogle Scholar
  119. Thurberg BL, Maloney CL, Vaccaro C, Afonso K, Tsai AC-H, Bossen E, Kishnani PS, O’Callaghan M (2006) Characterization of pre-and post-treatment pathology after enzyme replacement therapy for Pompe disease. Lab Investig 86(12):1208PubMedCrossRefPubMedCentralGoogle Scholar
  120. Tishchenko S, Gabdulkhakov A, Melnik B, Kudryakova I, Latypov O, Vasilyeva N, Leontievsky A (2016) Structural studies of component of lysoamidase bacteriolytic complex from Lysobacter sp. XL1. Protein J 35(1):44–50PubMedCrossRefPubMedCentralGoogle Scholar
  121. Tiwari R, Nain L, Labrou NE, Shukla P (2018) Bioprospecting of functional cellulases from metagenome for second generation biofuel production: a review. Crit Rev Microbiol 44(2):244–257PubMedCrossRefPubMedCentralGoogle Scholar
  122. Torchilin VP, Maksimenko AV, Smirknov VN, Berezin IV, Klibanov AM, Martinek K (1978) The principles of enzyme stabilization. III. The effect of the length of intra-molecular cross-linkages on thermostability of enzymes. Biochim Biophys Acta (BBA)-Enzymol 522(2):277–283CrossRefGoogle Scholar
  123. Tsuruta LR, Lopes dos Santos M, Moro AM (2015) Biosimilars advancements: moving on to the future. Biotechnol Prog 31(5):1139–1149PubMedPubMedCentralCrossRefGoogle Scholar
  124. Usmani SS, Bedi G, Samuel JS, Singh S, Kalra S, Kumar P, Ahuja AA, Sharma M, Gautam A, Raghava GPS (2017) THPdb: database of FDA-approved peptide and protein therapeutics. PLoS One 12(7):e0181748PubMedPubMedCentralCrossRefGoogle Scholar
  125. Vereshchagin IA, Vereshchagin SI, Zhuravleva OD (1985) Enhanced effectiveness of antibiotic therapy with an exogenous lysozyme in dysentery in children. Antibiot Med Biotekhnologiia Antibiot Med Biotechnol 30(12):927–931Google Scholar
  126. Vidya J, Ushasree MV, Pandey A (2014) Effect of surface charge alteration on stability of l-asparaginase II from Escherichia sp. Enzym Microb Technol 56:15–19CrossRefGoogle Scholar
  127. Vivian JT, Callis PR (2001) Mechanisms of tryptophan fluorescence shifts in proteins. Biophys J 80(5):2093–2109PubMedPubMedCentralCrossRefGoogle Scholar
  128. Wang D, Ichiyama RM, Zhao R, Andrews MR, Fawcett JW (2011) Chondroitinase combined with rehabilitation promotes recovery of forelimb function in rats with chronic spinal cord injury. J Neurosci 31(25):9332–9344PubMedPubMedCentralCrossRefGoogle Scholar
  129. Wang H, Hagedorn J, Svendsen A, Borch K, Otzen DE (2013) Variant of the Thermomyces lanuginosus lipase with improved kinetic stability: a candidate for enzyme replacement therapy. Biophys Chem 172:43–52PubMedCrossRefPubMedCentralGoogle Scholar
  130. Wang B, Ji SQ, Ma XQ, Lu M, Wang LS, Li FL (2018) Substitution of one calcium-binding amino acid strengthens substrate binding in a thermophilic alginate lyase. FEBS Lett 592(3):369–379PubMedCrossRefPubMedCentralGoogle Scholar
  131. Wen Z-Q (2007) Raman spectroscopy of protein pharmaceuticals. J Pharm Sci 96(11):2861–2878CrossRefPubMedGoogle Scholar
  132. Wong SS, Wong L-JC (1992) Chemical crosslinking and the stabilization of proteins and enzymes. Enzym Microb Technol 14(11):866–874CrossRefGoogle Scholar
  133. Wu XC, Ye R, Duan Y, Wong S-L (1998) Engineering of plasmin-resistant forms of streptokinase and their production in Bacillus subtilis: streptokinase with longer functional half-life. Appl Environ Microbiol 64(3):824–829PubMedPubMedCentralGoogle Scholar
  134. Yoo EH, Lee SY (2010) Glucose biosensors: an overview of use in clinical practice. Sensors 10(5):4558–4576PubMedCrossRefPubMedCentralGoogle Scholar
  135. Zenatti PP, Migita NA, Cury NM, Mendes-Silva RA, Gozzo FC, de Campos-Lima PO, Yunes JA, Brandalise SR (2018) Low bioavailability and high immunogenicity of a new brand of E. coli-asparaginase with active host contaminating proteins. EBioMedicine 30:158–166PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Shubhrima Ghosh
    • 1
  • Shahenvaz Alam
    • 1
  • Anurag S. Rathore
    • 2
  • S. K. Khare
    • 1
    Email author
  1. 1.Enzyme and Microbial Biochemistry Laboratory, Department of ChemistryIndian Institute of Technology DelhiNew DelhiIndia
  2. 2.Department of Chemical EngineeringIndian Institute of Technology DelhiNew DelhiIndia

Personalised recommendations