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中国生物工程杂志

China Biotechnology
China Biotechnology
China Biotechnology  2021, Vol. 41 Issue (9): 92-100    DOI: 10.13523/j.cb.2106041
    
Advances of the Physiochemical Properties of Sporopollenin and Its Biomedical Applications
SUN Li-ping1,**(),XU Wan1,LI Meng-wei1,ZENG Ru2,WENG Jian1
1 Key Laboratory of Biomedical Engineering of Fujian Province, Department of Biomaterials, College of Materials, Xiamen University, Xiamen 361005, China
2 Department of Medical Oncology, The First Affiliated Hospital of Xiamen University, Xiamen 361003, China
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Abstract  

Sporopollenin (SP) is a highly cross-linked natural biopolymer composed of polyvinyl alcohol-like unit crosslinked through ester and acetal linkage. SP forms the outer wall of pollen and spore and can resist physical, chemical and biological corrosion. It is the most robust organic compound in nature and is known as the diamond of plant kingdom. Sporopollenin exine capsules (SEC) are abundant in nature. They have good biocompatibility and no immunity. The rich carboxyl, hydroxyl and phenolic groups make SEC easy to be functionalized or complexed with nanomaterials. The plentiful nanochannels on SEC increases their specific surface area, supporting capture of cancer cell and biomolecules. The unique properties of SEC lead to their wide applications in drug delivery carriers, oral vaccine carriers, medical imaging, biosensing, cell growth scaffold, microreactor, micro robot, etc. In this review, the physicochemical properties, preparation methods and functionalization of SP as well as the research progress of SEC are discussed. The application prospect, existing problems and future development direction of SEC are summarized.

Key words： Sporopollenin      Pollen      Spore      Microcapsule      Drug carrier     
Received: 25 June 2021      Published: 30 September 2021
ZTFLH:  Q819  
Corresponding Authors: Li-ping SUN     E-mail: sunliping@xmu.edu.cn
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Li-ping SUN
Wan XU
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Cite this article:

SUN Li-ping,XU Wan,LI Meng-wei,ZENG Ru,WENG Jian. Advances of the Physiochemical Properties of Sporopollenin and Its Biomedical Applications. China Biotechnology, 2021, 41(9): 92-100.

URL:

https://manu60.magtech.com.cn/biotech/10.13523/j.cb.2106041     OR     https://manu60.magtech.com.cn/biotech/Y2021/V41/I9/92

Fig. 1 The structure of the cross section of pollen (a) The cross section of a pollen The external layer is marked blue, while the inner layer is marked yellow[4] (b) The nano channels in the external layer of SEC[5]
Fig.2 The surface morphology and chemical structure of sporopollenin (a) Scanning microscope image of SEC[3] (b) The average molecular structure of pine SP[7]
Fig.3 The preparation process of the sporopollenin exine capsule
Fig.4 Application of sporopollenin microcapsule in biomedicine (a) Optical image of DOX-loaded Pt-pollen microrobots[22] (b) Fluorescence image of DOX-loaded Pt-pollen microrobots[22] (c) Cell viability results of MCF-7 cells for DOX-loaded Pt-pollen microrobots[22] (d) In vitro release of BSA[14] (e) Release of the gadolinium contrast agent[30]
Fig.5 Detection of PSA using sporopollenin exine capsule-based biosensor (a) The rGO-modified SEC biosensor fabrication procedure (b) Dose-dependent responses to target PSA (c) Response time of rGO-SEC biosensor detection against 1×10-12 mol/L target PSA[38]
Fig.6 Capture of cancer cells using sporopollenin exine capsule (a) TEM image of a captured MCF-7 cell on EChry film (b) Schematic illustration of the filopodia of cancer cell stuck into the nanocage (c) The number of MCF-7 cells captured on EChry film as a function of loaded cell number (d) Capture yields of various cancer cells on EChry film[40]
[1]   Park J H, Seo J, Jackman J A, et al. Inflated sporopollenin exine capsules obtained from thin-walled pollen. Scientific Reports, 2016, 6:28017.
doi: 10.1038/srep28017
[2]   Krienitz L, Takeda H, Hepperle D. Ultrastructure, cell wall composition, and phylogenetic position of Pseudodictyosphaerium jurisii (Chlorococcales, Chlorophyta) including a comparison with other picoplanktonic green algae. Phycologia, 1999, 38(2):100-107.
doi: 10.2216/i0031-8884-38-2-100.1
[3]   Mundargi R C, Potroz M G, Park J H, et al. Eco-friendly streamlined process for sporopollenin exine capsule extraction. Scientific Reports, 2016, 6:19960.
doi: 10.1038/srep19960
[4]   Halbritter H, Ulrich S, Grímsson F, et al. Pollen morphology and ultrastructure. Illustrated pollen terminology. Cham: Springer International Publishing, 2018: 37-65.
[5]   Khare A R, Vasisht N. Nanoencapsulation in the food industry. Microencapsulation in the food industry. Amsterdam: Elsevier, 2014: 151-155.
[6]   Brooks J, Shaw G. Sporopollenin: a review of its chemistry, palaeochemistry and geochemistry. Grana, 1978, 17(2):91-97.
doi: 10.1080/00173137809428858
[7]   Li F S, Phyo P, Jacobowitz J, et al. The molecular structure of plant sporopollenin. Nature Plants, 2019, 5(1):41-46.
doi: 10.1038/s41477-018-0330-7
[8]   Sylvain B. Physical and chemical properties of sporopollenin exine particles. Hull: University of Hull, 2008.
[9]   Jardine P E, Fraser W T, Lomax B H, et al. The impact of oxidation on spore and pollen chemistry. Journal of Micropalaeontology, 2015, 34(2):139-149.
doi: 10.1144/jmpaleo2014-022
[10]   Southworth D. Solubility of pollen exines. American Journal of Botany, 1974, 61(1):36-44.
doi: 10.1002/j.1537-2197.1974.tb06025.x
[11]   Bernard S, Benzerara K, Beyssac O, et al. Evolution of the macromolecular structure of sporopollenin during thermal degradation. Heliyon, 2015, 1(2):e00034.
doi: 10.1016/j.heliyon.2015.e00034
[12]   Montgomery W, Potiszil C, Watson J S, et al. Sporopollenin, a natural copolymer, is robust under high hydrostatic pressure. Macromolecular Chemistry and Physics, 2016, 217(22):2494-2500.
doi: 10.1002/macp.v217.22
[13]   Rowley J, Skvarla J. The elasticity of the exine. Grana, 2000, 39(1):1-7.
doi: 10.1080/00173130150503759
[14]   Potroz M G, Mundargi R C, Gillissen J J, et al. Drug delivery: plant-based hollow microcapsules for oral delivery applications: toward optimized loading and controlled release. Advanced Functional Materials, 2017, 27(31):1700270. DOI: 10.1002/adfm.201770184.
doi: 10.1002/adfm.201770184
[15]   MacKenzie G, Boa A N, Diego-Taboada A, et al. Sporopollenin, the least known yet toughest natural biopolymer. Frontiers in Materials, 2015, 2:1-5.
[16]   Diego-Taboada A, Beckett S, Atkin S, et al. Hollow pollen shells to enhance drug delivery. Pharmaceutics, 2014, 6(1):80-96.
doi: 10.3390/pharmaceutics6010080 pmid: 24638098
[17]   Luo S X, Li Y Q, Chen S, et al. Gelechiidae moths are capable of chemically dissolving the pollen of their host plants: first documented sporopollenin breakdown by an animal. PLoS One, 2011, 6(4):e19219.
doi: 10.1371/journal.pone.0019219
[18]   Ahokas H. Evidence of a pollen esterase capable of hydrolyzing sporopollenin. Experientia, 1976, 32(2):175-177.
doi: 10.1007/BF01937750
[19]   Prabhakar A K, Lai H Y, Potroz M G, et al. Chemical processing strategies to obtain sporopollenin exine capsules from multi-compartmental pine pollen. Journal of Industrial and Engineering Chemistry, 2017, 53:375-385.
doi: 10.1016/j.jiec.2017.05.009
[20]   Tan E L, Potroz M G, Ferracci G, et al. Functionalized natural particles: light-induced surface modification of natural plant microparticles: toward colloidal science and cellular adhesion applications. Advanced Functional Materials, 2018, 28(18):1870120.
doi: 10.1002/adfm.v28.18
[21]   Tan E L, Potroz M G, Ferracci G, et al. Hydrophobic to superhydrophilic tuning of multifunctional sporopollenin for microcapsule and bio-composite applications. Applied Materials Today, 2020, 18:100525.
doi: 10.1016/j.apmt.2019.100525
[22]   Maric T, Nasir M Z M, Rosli N F, et al. Microrobots derived from variety plant pollen grains for efficient environmental clean up and as an anti-cancer drug carrier. Advanced Functional Materials, 2020, 30(19):2000112.
doi: 10.1002/adfm.v30.19
[23]   Wang H, Potroz M G, Jackman J A, et al. Micromotors: bioinspired spiky micromotors based on sporopollenin exine capsules. Advanced Functional Materials, 2017, 27(32):1702338. DOI: 10.1002/adfm.201770185.
doi: 10.1002/adfm.201770185
[24]   Wang Y T, Len T, Huang Y K, et al. Sulfonated sporopollenin as an efficient and recyclable heterogeneous catalyst for dehydration of d-xylose and xylan into furfural. ACS Sustainable Chemistry & Engineering, 2017, 5(1):392-398.
[25]   Wang L L, Ng W, Jackman J A, et al. Biosensors: graphene-functionalized natural microcapsules: modular building blocks for ultrahigh sensitivity bioelectronic platforms. Advanced Functional Materials, 2016, 26(13):2220.
doi: 10.1002/adfm.201670083
[26]   Wang L L, Jackman J A, Tan E L, et al. High-performance, flexible electronic skin sensor incorporating natural microcapsule actuators. Nano Energy, 2017, 36:38-45.
doi: 10.1016/j.nanoen.2017.04.015
[27]   王开发, 花粉的功能与应用. 北京: 化学工业出版社, 2004.
[27]   Wang K F. The function and application of pollen. Beijing: Chemical Industry Press, 2004.
[28]   Barrier S, Diego-Taboada A, Thomasson M J, et al. Viability of plant spore exine capsules for microencapsulation. J Mater Chem, 2011, 21(4):975-981.
[29]   Wakil A, MacKenzie G, Diego-Taboada A, et al. Enhanced bioavailability of eicosapentaenoic acid from fish oil after encapsulation within plant spore exines as microcapsules. Lipids, 2010, 45(7):645-649.
doi: 10.1007/s11745-010-3427-y
[30]   Akyuz L, Sargin I, Kaya M, et al. A new pollen-derived microcarrier for pantoprazole delivery. Materials Science & Engineering C, Materials for Biological Applications, 2017, 71:937-942.
doi: 10.1016/j.msec.2016.11.009
[31]   Diego-Taboada A, Maillet L, Banoub J H, et al. Protein free microcapsules obtained from plant spores as a model for drug delivery: ibuprofen encapsulation, release and taste masking. J Mater Chem B, 2013, 1(5):707-713.
doi: 10.1039/c2tb00228k pmid: 32260776
[32]   Mundargi R C, Tan E L, Seo J, et al. Encapsulation and controlled release formulations of 5-fluorouracil from natural Lycopodium clavatum spores. Journal of Industrial and Engineering Chemistry, 2016, 36:102-108.
doi: 10.1016/j.jiec.2016.01.022
[33]   Uddin M J, Gill H S. From allergen to oral vaccine carrier: a new face of ragweed pollen. International Journal of Pharmaceutics, 2018, 545(1-2):286-294.
doi: 10.1016/j.ijpharm.2018.05.003
[34]   Mundargi R C, Potroz M G, Park S, et al. Drug delivery: Lycopodium spores: a naturally manufactured, superrobust biomaterial for drug delivery (adv. funct. mater. 4/2016). Advanced Functional Materials, 2016, 26(4):632.
doi: 10.1002/adfm.201670027
[35]   Hamad S A, Dyab A F K, Stoyanov S D, et al. Encapsulation of living cells into sporopollenin microcapsules. Journal of Materials Chemistry, 2011, 21(44):18018.
doi: 10.1039/c1jm13719k
[36]   Sudareva N, Suvorova O, Saprykina N, et al. Two-level delivery systems for oral administration of peptides and proteins based on spore capsules of Lycopodium clavatum. Journal of Materials Chemistry B, 2017, 5(37):7711-7720.
doi: 10.1039/c7tb01681f pmid: 32264372
[37]   Lorch M, Thomasson M J, Diego-Taboada A, et al. MRI contrast agent delivery using spore capsules: controlled release in blood plasma. Chemical Communications (Cambridge, England), 2009(42):6442-6444.
[38]   Wang L L, Jackman J A, Ng W B, et al. Flexible, graphene-coated biocomposite for highly sensitive, real-time molecular detection. Advanced Functional Materials, 2016, 26(47):8623-8630.
doi: 10.1002/adfm.v26.47
[39]   Zhang Y B, Zhang L, Yang L D, et al. Real-time tracking of fluorescent magnetic spore-based microrobots for remote detection of C. diff toxins. Science Advances, 2019, 5(1): eaau9650. DOI: 10.1126/sciadv.aau9650.
doi: 10.1126/sciadv.aau9650
[40]   Jiang W N, Han L L, Yang L W, et al. Natural fish trap-like nanocage for label-free capture of circulating tumor cells. Advanced Science (Weinheim, Baden Wurttemberg, Germany), 2020, 7(22):2002259.
[41]   Ahmad N F, Kamboh M A, Nodeh H R, et al. Synthesis of piperazine functionalized magnetic sporopollenin: a new organic-inorganic hybrid material for the removal of lead(II) and arsenic(III) from aqueous solution. Environmental Science and Pollution Research, 2017, 24(27):21846-21858.
doi: 10.1007/s11356-017-9820-9
[42]   Yaacob S F F S, Razak N S A, Aun T T, et al. Synthesis and characterizations of magnetic bio-material sporopollenin for the removal of oil from aqueous environment. Industrial Crops and Products, 2018, 124:442-448.
doi: 10.1016/j.indcrop.2018.08.024
[43]   Fan T F, Potroz M G, Tan E L, et al. Species-specific biodegradation of sporopollenin-based microcapsules. Scientific Reports, 2019, 9(1):9626.
doi: 10.1038/s41598-019-46131-w
[44]   Atwe S U, Ma Y Z, Gill H S. Pollen grains for oral vaccination. Journal of Controlled Release, 2014, 194:45-52.
doi: 10.1016/j.jconrel.2014.08.010
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