Antimicrobial peptide-loaded decellularized placental sponge as an excellent antibacterial skin substitute against XDR clinical isolates

Amino Acids - Tập 55 - Trang 955-967 - 2023
Hatef Ghasemi Hamidabadi1,2, Sanaz Alizadeh3,4, Leila Mahboobi3, Zahra Khosrowpour3,4,5, Maryam Nazm Bojnordi1,2, Zahra Aliakbar Ahovan6, Majid Malekzadeh Shafaroudi1,2, Maria Zahiri7,8, Narendra Pal Singh Chauhan9, Mazaher Gholipourmalekabadi3,4,10
1Department of Anatomy & Cell Biology, Faculty of Medicine, Mazandaran University of Medical Sciences, Sari, Iran
2Immunogenetic Research Center, Department of Anatomy & Cell Biology, Faculty of Medicine, Mazandaran University of Medical Sciences, Sari, Iran
3Cellular and Molecular Research Centre, Iran University of Medical Sciences, Tehran, Iran
4Department of Tissue Engineering & Regenerative Medicine, Faculty of Advanced Technologies in Medicine, Iran University of Medical Sciences, Tehran, Iran
5Department of Pediatrics, University of Minnesota, Minneapolis, USA
6Department of Microbiology, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran
7The Persian Gulf Marine Biotechnology Research Center, The Persian Gulf Biomedical Sciences Research Institute, Bushehr University of Medical Sciences, Bushehr, Iran
8Department of Anatomical Sciences, School of Medical Sciences, Bushehr University of Medical Sciences, Bushehr, Iran
9Department of Chemistry, Faculty of Science, Bhupal Nobles’University, Udaipur, India
10Department of Medical Biotechnology, Faculty of Allied Medicine, Iran University of Medical Sciences, Tehran, Iran

Tóm tắt

Post-wound infections have remained a serious threat to society and healthcare worldwide. Attempts are still being made to develop an ideal antibacterial wound dressing with high wound-healing potential and strong antibacterial activity against extensively drug-resistant bacteria (XDR). In this study, a biological-based sponge was made from decellularized human placenta (DPS) and then loaded with different concentrations (0, 16 µg/mL, 32 µg/mL, 64 µg/mL) of an antimicrobial peptide (AMP, CM11) to optimize an ideal antibacterial wound dressing. The decellularization of DPS was confirmed by histological evaluations and DNA content assay. The DPS loaded with different contents of antimicrobial peptides (AMPs) showed uniform morphology under a scanning electron microscope (SEM) and cytobiocompatibility for human adipose tissue-derived mesenchymal stem cells. Antibacterial assays indicated that the DPS/AMPs had antibacterial behavior against both standard strain and XDR Acinetobacter baumannii in a dose-dependent manner, as DPS loaded with 64 µg/mL showed the highest bacterial growth inhibition zone and elimination of bacteria under SEM than DPS alone and DPS loaded with 16 µg/mL and 32 µg/mL AMP concentrations. The subcutaneous implantation of all constructs in the animal model demonstrated no sign of acute immune system reaction and graft rejection, indicating in vivo biocompatibility of the scaffolds. Our findings suggest the DPS loaded with 64 µg/mL as an excellent antibacterial skin substitute, and now promises to proceed with pre-clinical and clinical investigations.

Tài liệu tham khảo

Ahovan ZA, Khosravimelal S, Eftekhari BS, Mehrabi S, Hashemi A, Eftekhari S, Milan PB, Mobaraki M, Seifalian AM, Gholipourmalekabadi M (2020) Thermo-responsive chitosan hydrogel for healing of full-thickness wounds infected with XDR bacteria isolated from burn patients: In vitro and in vivo animal model. Int J Biol Macromol 164:4475–4486 Alizadeh S, Farshi P, Farahmandian N, Ahovan ZA, Hashemi A, Majidi M, Azadbakht A, Darestanifarahani M, Sepehr KS, Kundu SC (2022) Synergetic dual antibiotics-loaded chitosan/poly (vinyl alcohol) nanofibers with sustained antibacterial delivery for treatment of XDR bacteria-infected wounds. Int J Biol Macromol. https://doi.org/10.1016/j.ijbiomac.2022.11.288 Amani J, Barjini KA, Moghaddam MM, Asadi A (2015) In vitro synergistic effect of the CM11 antimicrobial peptide in combination with common antibiotics against clinical isolates of six species of multidrug-resistant pathogenic bacteria. Protein Pept Lett 22:940–951 Asgari F, Asgari HR, Najafi M, Eftekhari BS, Vardiani M, Gholipourmalekabadi M, Koruji M (2021a) Optimization of decellularized human placental macroporous scaffolds for spermatogonial stem cells homing. J Mater Sci Mater Med 32:1–17 Asgari F, Khosravimelal S, Koruji M, Ahovan ZA, Shirani A, Hashemi A, Hamidabadi HG, Chauhan NPS, Moroni L, Reis RL (2021b) Long-term preservation effects on biological properties of acellular placental sponge patches. Mater Sci Eng C 121:111814 Azad ZM, Moravej H, Fasihi-Ramandi M, Masjedian F, Nazari R, Mirnejad R, Moghaddam MM (2017) In vitro synergistic effects of a short cationic peptide and clinically used antibiotics against drug-resistant isolates of Brucella melitensis. J Med Microbiol 66:919–926 Azadbakht A, Alizadeh S, Ahovan ZA, Khosrowpour Z, Majidi M, Pakzad S, Shojaei S, Chauhan NPS, Jafari M, Gholipourmalekabadi M (2022) Chitosan-placental ECM composite thermos-responsive hydrogel as a biomimetic wound dressing with angiogenic property. Macromol Biosci 23:2200386 Benders KEM, van Weeren PR, Badylak SF, Saris DBF, Dhert WJA, Malda J (2013) Extracellular matrix scaffolds for cartilage and bone regeneration. Trends Biotechnol 31:169–176 Chizari M, Khosravimelal S, Tebyaniyan H, Moosazadeh Moghaddam M, Gholipourmalekabadi M (2022) Fabrication of an antimicrobial peptide-loaded silk fibroin/gelatin bilayer sponge to apply as a wound dressing; an in vitro study. Int J Pept Res Ther 28:1–13 Choi JS, Kim JD, Yoon HS, Cho YW (2013) Full-thickness skin wound healing using human placenta-derived extracellular matrix containing bioactive molecules. Tissue Eng Part A 19:329–339. https://doi.org/10.1089/ten.tea.2011.0738 Farshi P, Salarian R, Rabiee M, Alizadeh S, Gholipourmalekabadi M, Ahmadi S, Rabiee N (2022) Design, preparation, and characterization of silk fibroin/carboxymethyl cellulose wound dressing for skin tissue regeneration applications. Polym Eng Sci 62:2741 Fjell CD, Hiss JA, Hancock REW, Schneider G (2012) Designing antimicrobial peptides: form follows function. Nat Rev Drug Discov 11:37–51 Gholipourmalekabadi M, Sameni M, Radenkovic D, Mozafari M, Mossahebi-Mohammadi M, Seifalian A (2016) Decellularized human amniotic membrane: how viable is it as a delivery system for human adipose tissue-derived stromal cells? Cell Prolif 49:115–121 Gholipourmalekabadi M, Khosravimelal S, Nokhbedehghan Z, Sameni M, Jajarmi V, Urbanska AM, Mirzaei H, Salimi M, Chauhan NPS, Mobaraki M (2019) Modulation of hypertrophic scar formation using amniotic membrane/electrospun silk fibroin bilayer membrane in a rabbit ear model. ACS Biomater Sci Eng 5:1487–1496 Greco I, Molchanova N, Holmedal E, Jenssen H, Hummel BD, Watts JL, Håkansson J, Hansen PR, Svenson J (2020) Correlation between hemolytic activity, cytotoxicity and systemic in vivo toxicity of synthetic antimicrobial peptides. Sci Rep 10:1–13 Hamidabadi HG, Simorgh S, Kamrava SK, Namjoo Z, Bagher Z, Bojnordi MN, Niapour A, Mojaverrostami S, Saeb MR, Zarrintaj P (2021) Promoting motor functions in a spinal cord injury model of rats using transplantation of differentiated human olfactory stem cells: a step towards future therapy. Behav Brain Res 405:113205 He Y, Jin Y, Ying X, Wu Q, Yao S, Li Y, Liu H, Ma G, Wang X (2020) Development of an antimicrobial peptide-loaded mineralized collagen bone scaffold for infective bone defect repair. Regen Biomater 7:515–525 Hsueh P-R, Ko W-C, Wu J-J, Lu J-J, Wang F-D, Wu H-Y, Wu T-L, Teng L-J (2010) Consensus statement on the adherence to Clinical and Laboratory Standards Institute (CLSI) antimicrobial susceptibility testing guidelines (CLSI-2010 and CLSI-2010-update) for enterobacteriaceae in clinical microbiology laboratories in Taiwan. J Microbiol Immunol Infect 43:452–455 Khosrowpour Z, Hashemi SM, Mohammadi-Yeganeh S, Moghtadaei M, Brouki Milan P, Moroni L, Kundu SC, Gholipourmalekabadi M (2023) Coculture of adipose-derived mesenchymal stem cells/macrophages on decellularized placental sponge promotes differentiation into the osteogenic lineage. Artif Organs 47:47 Leekha, S., Terrell, C.L., Edson, R.S., 2011. General principles of antimicrobial therapy, in: Mayo Clinic Proceedings. Elsevier, pp. 156–167. Li W, Separovic F, O’Brien-Simpson NM, Wade JD (2021) Chemically modified and conjugated antimicrobial peptides against superbugs. Chem Soc Rev 50:4932–4973 Mahlapuu M, Håkansson J, Ringstad L, Björn C (2016) Antimicrobial peptides: an emerging category of therapeutic agents. Front Cell Infect Microbiol 6:194 Miao F, Li Y, Tai Z, Zhang Y, Gao Y, Hu M, Zhu Q (2021) Antimicrobial peptides: the promising therapeutics for cutaneous wound healing. Macromol Biosci 21:2100103 Moghaddam MM, Abolhassani F, Babavalian H, Mirnejad R, Azizi Barjini K, Amani J (2012) Comparison of in vitro antibacterial activities of two cationic peptides CM15 and CM11 against five pathogenic bacteria: Pseudomonas aeruginosa, Staphylococcus aureus, Vibrio cholerae, Acinetobacter baumannii, and Escherichia coli. Probiotics Antimicrob Proteins 4:133–139 Moghaddam MM, Barjini KA, Ramandi MF, Amani J (2014) Investigation of the antibacterial activity of a short cationic peptide against multidrug-resistant Klebsiella pneumoniae and Salmonella typhimurium strains and its cytotoxicity on eukaryotic cells. World J Microbiol Biotechnol 30:1533–1540 Moosazadeh Moghaddam M, Eftekhary M, Erfanimanesh S, Hashemi A, Fallah Omrani V, Farhadihosseinabadi B, Lasjerdi Z, Mossahebi-Mohammadi M, Chauhan NPS, Seifalian AM (2018a) Comparison of the antibacterial effects of a short cationic peptide and 1% silver bioactive glass against extensively drug-resistant bacteria, Pseudomonas aeruginosa and Acinetobacter baumannii, isolated from burn patients. Amino Acids 50:1617–1628 Moosazadeh Moghaddam M, Eftekhary M, Erfanimanesh S, Hashemi A, Fallah Omrani V, Farhadihosseinabadi B, Lasjerdi Z, Mossahebi-Mohammadi M, Chauhan PSN, Seifalian AM (2018b) Consensus statement on the adherence to Clinical and Laboratory Standards Institute (CLSI) Antimicrobial Susceptibility Testing Guidelines (CLSI-2010 and CLSI-2010-update) for Enterobacteriaceae in clinical microbiology laboratories in Taiwan. J Amino Acids 50:1617–1628 Rameshbabu AP, Ghosh P, Subramani E, Bankoti K, Kapat K, Datta S, Maity PP, Subramanian B, Roy S, Chaudhury K (2016) Investigating the potential of human placenta-derived extracellular matrix sponges coupled with amniotic membrane-derived stem cells for osteochondral tissue engineering. J Mater Chem B 4:613–625 Rezaei N, Hamidabadi HG, Khosravimelal S, Zahiri M, Ahovan ZA, Bojnordi MN, Eftekhari BS, Hashemi A, Ganji F, Darabi S (2020) Antimicrobial peptides-loaded smart chitosan hydrogel: release behavior and antibacterial potential against antibiotic resistant clinical isolates. Int J Biol Macromol 164:855–862 Salick DA, Pochan DJ, Schneider JP (2009) Design of an injectable β-Hairpin peptide hydrogel that kills methicillin-resistant staphylococcus aureus. Adv Mater 21:4120–4123 Sander EA, Lynch KA, Boyce ST (2014) Development of the mechanical properties of engineered skin substitutes after grafting to full-thickness wounds. J Biomech Eng 136:51008 Simorgh S, Milan PB, Saadatmand M, Bagher Z, Gholipourmalekabadi M, Alizadeh R, Hivechi A, Arabpour Z, Hamidi M, Delattre C (2021) Human olfactory mucosa stem cells delivery using a collagen hydrogel: as a potential candidate for bone tissue Engineering. Materials (basel) 14:3909 Sun Z, Ma L, Sun X, Sloan AJ, O’Brien-Simpson NM, Li W (2023) The overview of antimicrobial peptide-coated implants against oral bacterial infections. Aggregate. https://doi.org/10.1002/agt2.309 Thapa RK, Diep DB, Tønnesen HH (2020) Topical antimicrobial peptide formulations for wound healing: Current developments and future prospects. Acta Biomater 103:52–67 Ullah H, Ali S (2017) Classification of anti-bacterial agents and their functions. Antibact Agents 10:1–16 Werner S, Grose R (2003) Regulation of wound healing by growth factors and cytokines. Physiol Rev 83:835–870 Yazdanpanah A, Madjd Z, Pezeshki-Modaress M, Khosrowpour Z, Farshi P, Eini L, Kiani J, Seifi M, Kundu SC, Ghods R (2022) Bioengineering of fibroblast-conditioned polycaprolactone/gelatin electrospun scaffold for skin tissue engineering. Artif Organs 46:1040–1054 Yu G, Baeder DY, Regoes RR, Rolff J (2018) Predicting drug resistance evolution: insights from antimicrobial peptides and antibiotics. Proc r Soc B Biol Sci 285:20172687 Zhang X, Chen X, Hong H, Hu R, Liu J, Liu C (2022) Decellularized extracellular matrix scaffolds: recent trends and emerging strategies in tissue engineering. Bioact Mater 10:15–31