A Comprehensive Review on Collagen Type I Development of Biomaterials for Tissue Engineering: From Biosynthesis to Bioscaffold
Abstract
:1. Introduction
2. Molecular Structure and Biosynthesis of Collagen Type I
2.1. Types of Collagens
2.2. Collagen Type I Supramolecular Structure
2.3. Collagen Type I Molecular Structure and Content
2.4. Biosynthesis
2.4.1. Transcription and Translation
2.4.2. Post-Translational Modifications
2.4.3. Collagen Secretion
2.4.4. Clinical Significance of Biosynthesis for Tissue Engineering
3. Sources of Collagen Type I
4. Extraction of Collagen Type I
4.1. Salting-Out Method
4.2. Acid Extraction Method
4.3. Alkali Extraction Method
4.4. Enzymatic Extraction Method
4.5. Ultrasound Extraction Method
4.6. Collagen Extraction Process
5. Physicochemical Characterisation of Collagen Type I
5.1. Parameters and Test Methodologies for Biomaterial Analysis
5.2. Characterisation of Purified Collagen Type I
5.3. Biocompatibility and Immunogenicity Properties of Collagen Type I
5.4. Three-Dimensional Stability
5.4.1. Mechanical Strength
5.4.2. Thermal Stability: Denaturing Temperature
5.4.3. Porosity and Pore Size
5.4.4. Biodegradation
5.5. Swelling Ratio
5.6. Water Vapour Transmission Rate
5.7. Surface Characteristics
5.8. Chemical Characteristics of Collagen Type I
5.8.1. X-ray Photoelectron Spectroscopy
5.8.2. Fourier Transform Infrared
5.8.3. Energy Dispersive X-ray
5.8.4. X-ray Diffraction
6. Current Insights and Conclusion
6.1. Current Insights over the Last Five Years
6.2. Trends and Future Perspectives
6.3. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Animal Class | Source and Tissue Type | Pre-Treatment Method | Extraction and Purification Method | Scaffold Comparisons | Reference |
---|---|---|---|---|---|
Mammalian | Human-placenta | Alkaline; 0.1 M NaOH in 1:10 (w/v) ratio; 6 h stir | Acid; 0.06 M acetic acid 1:25 (w/v) overnight; NaCl 3 M pH 7 to collect supernatant; dialysis against distilled water 5 days | -Cost effective (human waste) -Safe and fast extraction method | Karami et al., 2019 [91] |
Bovine skin, bone, pericardium | Alkaline; 300 mL of 0.1 M NaOH at 4 °C 48 h; filtered 3X | Acid–enzyme; 300 mL 10 mM HCl with pepsin to solution ratio of 1:20; pH 2.0 4 °C 12 h; urea and NaCl to collect supernatant; 1 M Tris for pepsin deactivation; dialysis against 1 M phosphate buffer 4 °C 16 h | -Collagen in the purified form -Can be a substitute/replaced from the commercial collagen -Simple extraction method | Santos et al., 2013 [92] | |
Rat tail | Salt; 10% NaCl 4 °C 24 h | Acid–enzyme; 0.5 M HCl and pepsin 1:50 4 °C 24 h; NaCl to collect supernatant and washed with phosphate buffer pH 7.4, 0.02 M | -Biocompatible -Induce contraction effect in in vitro model -Excellent for dental application | Techatanawat et al., 2011 [93] | |
Goat tendon | Acid; 1% (v/v) acetic acid 4 °C 72 h | Acid; 1% v/v after cotton mesh filtration and dialysis against 10 mM PBS 48 h, then further dialysed against 0.05 M Na2 HPO4 | -In vitro and in vivo study towards HUVEC cells showed prominent result -Good for future angiogenesis study | Banerjee et al., 2012 [94] | |
Sheep tendon | Acid; 0.35 M acetic acid 4 °C 24–48 h | Acid; 0.35 M acetic acid; NaCl salting-out 4 °C 24–48 h; supernatant undergoes dialysis against Na2HPO4 and PBS 14 kDa 4 °C 72 h | -Biocompatible toward human dermal fibroblasts (HDFs) -Greater availability and wider acceptability (religious views) -Can be fabricated into porous scaffolds | Fauzi et al., 2016 [71] | |
Fish | Freshwater fish scales | Salt; 1.0 M NaCl, 0.05 M Tris HCl, 20.0 mM EDTA 48 h (pH7.5); demineralisation 0.5 M EDTA 48 h (pH 7.4) | Acid; 0.5 M acetic acid (pH 2.5) 48 h; NaCl (0.9 M) salting-out 24 h; resolubilised supernatant undergoes dialysis against 0.1 M acetic acid and deionised water 24 h | -Cost effective -Alternative to other collagen sources -Highly biocompatible | Pati et al., 2012 [95] |
Bighead carp fins, scales, skin, bones, and swim bladders | Alkaline; 0.1 M NaOH 1:10 (w/v) ratio; 4 °C 36 h | Acid–enzyme; 0.5 M acetic acid 0.1% (w/v) pepsin 1:10 (w/v days; NaCl to collect supernatant 2 M; dialysis against distilled water 7 kda | -Alternative to other sources of collagen -Pepsin-solubilized collagen (PSC) can be extracted | Liu et al., 2012 [96] | |
Loach skin | Alkaline–salt; 10% NaCl 1:5 (w/v) 4 °C 1 h. 0.1 mol/L NaOH 1:10(w/v) 4 °C 24 h | Acid–enzyme; 0.5 mol/L acetic acid 1:30(w/v) 4 °C 24 h 5% (w/v) pepsin 2X; NaCl 0.9 mol/L to collect supernatant; dialysis against distilled water 8 kDa | -Alternative to other sources of collagen -Acid-soluble collagen (ASC) and pepsin-soluble collagen (PSC) can be extracted | Wang et al., 2018 [97] | |
Clown featherback skin | Alkaline; 0.1 M NaOH 1:15 (w/v) 4 °C 8 h | Acid–ultrasound; 0.5 M acetic acid 4 °C 48 h; in 30 min ultrasonication (20–80% between 10–30 min); NaCl to collect supernatant to 2.6 M; dialysis against distilled water for 2 days | -Ultrasonic application improves the extraction efficiency -Higher yield production, alternative to other collagen sources | Petcharat et al., 2020 [89] | |
Marine | Jumbo squid mantles | Acid; 6 M urea in sodium acetate (pH 6.8) and neutral buffer 24 h | Acid; 0.5 M acetic acid 24 h; supernatant collected for acid soluble collagen | -Acid-soluble collagen (ASC) can be extracted -Have some similar characteristics to bovine collagen | Uriarte-Montoya et al., 2010 [98] |
Jellyfish tissues | Acid; 0.5 M acetic acid | Acid–enzyme; 0.5 M acetic acid centrifuged and added pepsin (1–15 mg/mg tissue) overnight; NaCl (0.9 M) used to collect supernatant and dialysed against 0.1 M acetic acid | -Alternative to other sources of collagen -Biocompatible in in vitro testing | Addad et al., 2011 [99] | |
Jellyfish and squid | Acid; 0.5 M acetic acid 1:15 (w/v) 4 °C 3 days | Acid; 0.5 M acetic acid 1:15 (w/v) 4 °C 3 days after filtration through cheesecloth; NaCl (0.9 M) and 0.05 M Tris and used to collect supernatant and dialysed against 0.1 M acetic acid 3 days and distilled water another 3 days | -Alternative to other sources of collagen -Pepsin-soluble collagen (PSC) can be extracted | Jankangram et al., 2016 [100] | |
Amphibian | Bullfrog fallopian tubes | Alkali; 0.1 M NaOH 4 °C 1 day | Acid–enzyme; 0.5 M acetic acid with 10% pepsin 4 °C 2 days; NaCl (0.7 M) to collect supernatant; resolubilised acid solution dialysed against 0.1 M acetic acid 1 day; distilled water 2 days | -Pepsin-soluble collagen (PSC) can be extracted -Potential alternative and supplements from other sources of collagen | Wang et al., 2011 [101] |
Avian | Skin, skin dermis | Acid (acetic acid) | Acid-based extraction (acetic acid); enzymatic method (pepsin) | -Non-immunogenic and non-allergenic -Biocompatible -Can be fabricated into porous scaffolds | Peng et al., 2010, Parenteau-Bareil et al. 2011 [102,103] |
Chicken cartilage | Acid (EDTA) | Salting-out (NaCl) + ultrasound | -Increased yield production through ultrasound -Pepsin-soluble collagen (PSC) can be extracted | Akram and Zhang, 2020 [88] | |
Chicken lungs | Acid salt (sodium carbonate) | Acid extraction (acetic acid) + salting-out (NaCl) + enzymatic method (pepsin) + ultrasound | -Increased yield production through ultrasound -Alternative source to mammalian collagen -Higher thermal stability | Zou et al., 2020 [87] |
Characterisation | Method | Expectation | Reference |
---|---|---|---|
Biocompatibility | |||
Biocompatibility and immunogenicity | MTT assay Live/dead assay Cell attachment Immunocytochemistry (ICC) | Cell proliferation and growth; SEM; more than 80% cell adhesion after 24 h; integrin-related protein expression and cell attachment | Addad et al., 2011 [99], Fauzi et al., 2016 [71], Fauzi et al., 2017 [104], Thievessen et al., 2015 [105] |
Physical, Morphological, and Topographical (PMT) Characterisation for Three-dimensional stability | |||
Weight | SDS-PAGE | Type I collagen is composed of β (250 kDa), α1 (130 kDa), and α2 (115 kDa) | Peng et al., 2010 [102], Parenteau-Bareil et al., 2010 [106], Fauzi et al., 2016 [71] Inanc et al., 2017 [107] |
Native conformation | UV-circular dichroism (CD) spectroscopy | CD with a positive maximum absorption band at around 222 nm | Carvalho et al., 2018 [108] |
Mechanical strength | Tensile strength and Young’s modulus | No gold standard, but fish and reptile should be more fragile than mammalian material | Amri et al. 2014 [109], Teramoto et al. 2012 [110] |
Thermal stability | Thermogravimetry analysis (TGA) Differential scanning calorimetry (DSC) | No gold standard for what Td of biomaterial should be, but it must be stable to use normal temperatures or higher; in general, comparable or higher than native rat tail tendon collagen fibre Td of 65 °C; Td of extracted collagen in solution are 37–40 °C, 26- °C, and 6–20 °C, for mammalians, fish, and deep-sea animals, respectively | Miles and Bailey 1999 [111], Zhang et al., 2020 [112], Subhan et al., 2015 [113], Bozec and Odlyha, 2011 [114] |
Porosity and pore size | SEM | Pore size > 80 µm for fibrogenic and <20 µm for chondrogenic growth; the average mean size for ovine-, bovine-, and porcine-derived scaffolds are 73.05 ± 10.79 µm, 85.84 ± 9.51 µm, and 87.32 ± 10.69 µm, respectively | Ghodbane and Dunn 2016 [115] |
Biodegradation | Enzymatic biodegradation method | Depends on application example within 14 days for cutaneous wound healing | Mh Busra et al., 2019 [116] Salleh et al., 2022 [117] |
Swelling ratio | Swelling ratio protocol | 1000–2700% for biomaterials | Ghodbane and Dunn 2016 [115] |
Water vapor transmission rate (WVTR) | WVTR method | Within range 2028.3 ± 237.8 g/m2/day to maintain a moist environment and enhance the normal healing phase | Xu et al., 2016 [118] |
Surface and particle physicality | Contact angle zeta potential | Angle < 90° hydrophilic; isoelectric points (pIs) close to 6 at zero zeta potential | Chen et al., 2019 [119] |
Chemical Characterisation | |||
X-ray photoelectron spectroscopy (XPS) | XPS | Samples should show ≈0.1 atomic % as nominal sensitivity with an elemental sensitivity that may differ as much as ≈100; for the assessment of chemical components, a sample size larger than ≈10 μm will be convenient | Baer et al., 2019 [120] |
Fourier transform infrared (FTIR) | FTIR | Collagen type I functional groups include amides I, II, and III; range of peak intensity between 1450 cm−1 and 1235 cm−1 commonly indicates the helical structure of collagen; amide A at the higher peak intensity of 3350 cm−1 can be attributed to collagen type I; At peak intensity of 1632 cm−1, this indicates the higher-order arrangement of the collagen structure, which refers to β-sheet and triple helix structure | Sasmal and Begam 2014 [121] Fauzi et al., 2016 [71] |
Energy dispersive X-ray (EDX) | EDX | Major elements in collagen type 1 are oxygen, nitrogen, and carbon with a higher percentage of oxygen, followed by nitrogen and carbon | Fauzi et al., 2014 [122] |
X-ray diffraction (XRD). | XRD | Collagen XRD generally consists of 2 clear peaks, where the first peak is sharper than the second peak; collagen type I from different sources of mammalian, avian, marine, fish, etc., via XRD has been proven closer to the amorphous phase rather than crystallinity | Zhang et al., 2011 [123], Fauzi et al., 2016 [71], León-Mancilla et al., 2016 [124] |
Table | Mechanism | Main Characteristics | ||
---|---|---|---|---|
Pros | Cons | |||
Physical | Dehydrothermal treatment (DHT) | Water is removed as amide bonds are formed between amine and carboxyl groups of collagens (inter-molecular). Lysino-alanine bonds are also formed between lysine residues and dehydro-alanine in collagen chains (intra-molecular) [112,144]. | Safe. Non-toxic to cells. Thermally stable. Sterilization. | May cause denaturation. Low collagenase resistance [153]. |
Ultraviolet irradiation (UV) | Non-ionizing irradiation to induce collagen amino acids residues—Trp, Phe, and Tyr—to generate free radicals to cause inter-molecular crosslinks [146]. | Rapid process. Non-toxic to cells. Sterilization. | May cause denaturation. Poor crosslinking strength. | |
Gamma ray/electron beams | Free radical mediation—hydroxyl radicals from amino acid residues—Phe, His, and Met—form intermolecular crosslinks [164]. Furthermore, two tyrosyl radicals can form dityrosine bonds and crosslink [165]. | |||
Chemical | Glutaraldehyde (GA) | Aldehydes crosslink collagen by forming Schiff bases between the ε-amino groups from lysine or hydroxylysine residues and the aldehyde groups of aldehyde [112]. | Low cost. High reactivity. High water solubility. | Potential cytotoxicity to cells. |
Dialdehyde starch | Low cytotoxicity. Biodegradable. Resistant to collagenase. | Costly. Sensitive to oxidation [166]. | ||
Epoxy compounds | Epoxy groups form multipoint crosslinking with ε-amino groups of lysyl residues at alkali condition [167]. | Makes tissues more pliable [168]. Biocompatible with corneal cells [152]. | Affected by pH [167]. | |
N-hydroxysuccinimide (NHS) | Carboxyl groups from polycarboxylic acids are turned into active ester groups, which then crosslink with free amino groups within different collagen chains [147]. | Highly resistant to collagenase [142]. | Requires thorough washing. | |
1-ethyl-3(3-dimethylaminopropyl)-carbodiimide (EDC) | Crosslinking via amido bond between carboxyl groups and amino groups in adjacent collagen chains. EDC activates carboxyl groups (Glu and Asp) into active O-acylisourea groups, which undergo nucleophilic attack by free amine groups (lys or hyl), forming amido bonds. Usually, NHS is added to catalyse the reaction (EDC/NHS crosslinking) [169,170]. | Stronger crosslinking effect. Zero-length crosslinker and intra-fibrillar. Low cytotoxicity. | Can cause excessive crosslinking and stiffness. | |
Diphenylphosphorylazide (DPPA) | Converts carboxyl groups into acylazide groups, which react with the free amino groups of adjacent collagen chains (amido bonds) [148]. | Fast. Non-toxic. Resistant to collagenase. | Difficult to remove solvent. | |
Biological | Genipin | Crosslinking by initiating a nucleophilic attack on amine with two amino groups. The genipin C3-atom undergoes nucleophilic attack from primary amine groups (lys, hyl, arg), which then reacts with another collagen amino group by replacing an oxygen on the genipin ring, forming a nitrogen–iridoid (heterocyclic compound). Two iridoids are linked through a radical reaction to form intramolecular and intermolecular crosslinks [155,156] | Natural resources, biocompatible with cells. Resistant to collagenase. | Excessive concentration will reduce scaffold mechanical strength. Blue reaction after crosslinking. Sensitive to light and oxidation. |
Transglutaminase (TG) | Catalysed γ-carboxamide groups of gln residues become the acyl donor for acyl receptors, which are the ε-amino groups of lys residues or primary amino groups. Then, ε-(γ-glutamyl) lysine bonds form intra- and intermolecular bonds [158]. | Non-toxic, good biocompatibility. Similar to natural crosslinking. | Enzyme deregulation may cause harmful diseases. | |
Plant polyphenols/procyanidin/proanthocyanidins (PA) | Multipoint hydrogen bonds formed between phenolic hydroxyl groups of polyphenols and hydroxyl, carboxyl, amino, or amide groups of collagen chains [162] | Very low cytotoxicity. Antioxidants. Anticancer, antimicrobial, antiangiogenic, and anti-inflammatory [163]. | Sensitivity to thermal treatment, light, and oxidation. |
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Amirrah, I.N.; Lokanathan, Y.; Zulkiflee, I.; Wee, M.F.M.R.; Motta, A.; Fauzi, M.B. A Comprehensive Review on Collagen Type I Development of Biomaterials for Tissue Engineering: From Biosynthesis to Bioscaffold. Biomedicines 2022, 10, 2307. https://doi.org/10.3390/biomedicines10092307
Amirrah IN, Lokanathan Y, Zulkiflee I, Wee MFMR, Motta A, Fauzi MB. A Comprehensive Review on Collagen Type I Development of Biomaterials for Tissue Engineering: From Biosynthesis to Bioscaffold. Biomedicines. 2022; 10(9):2307. https://doi.org/10.3390/biomedicines10092307
Chicago/Turabian StyleAmirrah, Ibrahim N., Yogeswaran Lokanathan, Izzat Zulkiflee, M. F. Mohd Razip Wee, Antonella Motta, and Mh Busra Fauzi. 2022. "A Comprehensive Review on Collagen Type I Development of Biomaterials for Tissue Engineering: From Biosynthesis to Bioscaffold" Biomedicines 10, no. 9: 2307. https://doi.org/10.3390/biomedicines10092307