Human Dental Pulp Stem Cells: Comparison
View Latest Version
Please note this is a comparison between Version 2 by Camila Xu and Version 1 by Nadia Lampiasi.

Human dental pulp stem cells (hDPSCs) are adult mesenchymal stem cells (MSCs) obtained from dental pulp and derived from the neural crest. They can differentiate into odontoblasts, osteoblasts, chondrocytes, adipocytes and nerve cells, and they play a role in tissue repair and regeneration.

  • hDPSCs
  • PIEZO1
  • ATP
  • migracytosis
  • blebbing

1. Introduction

Adult stem cells are a resource for living organisms that allow for the repair and/or regeneration of damaged tissues. In general, there are two different approaches to regenerate damaged tissue using stem cells: cell homing and cell transplantation, both of which imply cell migration. Mesenchymal stem cells (MSCs) are found mainly in the bone marrow (BM), but also in the adipose tissue and in the pulp of the tooth. They can give rise to osteoblasts, chondrocytes and adipocytes. Dental pulp stem cells (DPSCs) are unique because they arise from the ectomesodermal embryonic tissue that forms the neural crest. For this reason, in addition to the cell types described above, they can give rise to odontoblasts (specialized osteoblasts) and nerve cells (astrocytes, glia cells and oligodendrocytes). The microenvironment in which stem cells are found affects their differentiation. In the case of naïve DPSCs, the niches in which they are located are innervated, supplied with blood and inside a rigid structure (tooth). The decision between the renewal and migration/differentiation of DPSCs depends on their interactions with stromal cells and ECMs in the niches. Different niches possess different DPSCs. As an example, after tooth injury in the apical part of the pulp, there was a population of highly proliferative potential which was Notch2-positive [1], whereas in the perivascular niches, DPSCs were positive for Oct3/4 stemness markers [2]. It has been shown that in vivo human (h) DPSCs migrate and can repair dentin by regenerating damaged odontoblasts in the tooth [3]. Furthermore, hDPSCs transplanted into mice can promote bone regeneration in defective calvaria [4] or migrate to ischemic areas, i.e., areas of cerebral infarction, and express specific neural markers [5]. Additionally, when induced in vitro as neural cells, they can differentiate in vivo into mature neurons or astrocytes [6]. However, hDPSCs can also repair damaged nerve tissue through paracrine mechanisms involving chemotaxis and the proliferation of endogenous neural stem cells (NSCs) [7], or they can reduce ischemic damage through the inhibition of microglial activation and the expression of pro-inflammatory cytokines [8]. When comparing MSC transplantation with the practice of homing for tissue regeneration in preclinical animal models, the latter is safer and more effective [9].

2. HDPSCs

HDPSCs can be purified from dental pulp essentially by two methods. The first is based on the enzymatic digestion of the dental pulp with collagenase and dispase and/or trypsin [10] (Table 1).
Table 1. Schematic list of the manuscripts cited divided according to the DPSC recovery method.
Digestion Method Explant Method Not Specified Cell Line
[3] [1] [8] [11]
[5] [2] [12] [13]
[6] [7] [14] [15]
[10] [16] [17] [18]
[19] [20] [21] [22]
[23] [24]   [25]
[26] [27]   [23]
[20] [28]    
[27] [29]    
[30] [31]    
[32] [33]    
[34] [35]    
[36]      
[37]      
[38]      
[39]      
[40]      
[41]      
[42]      
[43]      
[44]      
[45]      
[46]      
[47]
The harvested cells were dispersed in the medium, plated and left to proliferate. In turn, they formed colonies of heterogeneous cells, including stem cells from various niches in a mixture, and epithelial cells, stromal cells, perivascular cells, etc. [19] (Figure 1A). In this regard, heterogeneous cells expanded in a serum-free medium produced two DPSC subtypes, those being adherent (ADH) and non-adherent (non-ADH) populations according to their differential adhesion to plastic; however, both populations displayed osteogenic and neurogenic differentiation [26,48][26][48]. The second method consisted of putting the pulp, or fragments, directly in a plate with a culture medium and waiting for the DPSCs to come out after about 10–15 days (explant method) (Table 1, Figure 1B and Figure 2A) [16]. The tissue piece is present during the primary culture and therefore, DPSCs reside in the dental niches with stromal cells and extracellular matrix (ECM), since no proteolytic enzymes are added in the culture. DPSCs take a long time to come out from the pulp, but they take advantage of the presence of other cells and the ECM. This method makes it possible to observe the cells that are induced to migrate. Indeed, DPSCs gradually emerge from the tissue, whereas non-migrating cells remain inside the tissue and can migrate later (for agreement with DPSCs residing in different niches, see [1], or if they are not stem cells, they undergo apoptosis [1,2,49][1][2][49]). However, DPSCs obtained by the explant method produce a more homogeneous population (i.e., subsequent waves, see [20]), and unattached and adherent cells, different from DPSCs, are present in the culture [24]. However, unattached cells will be gradually removed after refreshing the culture media, and adherent cells are unable to survive/proliferate and will be lost during the first few subcultures [20,49][20][49].
Biology 12 00742 g001
Figure 1. Description of the methods used to recover dental pulp stem cells: (A) digestion method, (B) explant method and (C) differentiation of DPSCs.
Biology 12 00742 g002
Figure 2. DPSCs harvested using the explant method from the third molar extracted for orthodontic reasons. Examples include: (A) DPSCs recovered by explant method (10×) (B,C) mesenchymal migration (20×), (D) FA (20×), (E) lamellipodia (20×), (F) filopodia (20×), (G) blebs and ameboid migration (20×), (H) migrasomes (20×). Light Microscopy (Zeiss Axio). DPSCs were isolated with the explant method from teeth removed for orthodontic reasons and the patients agreed to the use of their samples for research purposes. Bar = 20 µm; 50 µm.
Therefore, the two isolation methods yielded different subpopulations of cells, even though regardless of the recovery method, DPSCs showed the same trilineage differentiation potential when not pre-selecting for specific marker expressions [24,27,50][24][27][50]. In general, in vitro hDPSCs are most likely induced to migrate and proliferate following environmental cues such as chemical and biophysical stimuli, for example, changes in stiffness and rigidity (both are mechanical stimuli) [51,52][51][52]. However, in the explant method, a wound healing response is triggered due to the production of cytokines and factors released by the injured tissue, which promote migration [30,49][30][49]. Cells harvested with the explant method migrate as “leaders” and “followers”, where leaders migrate first as single cells [28,53][28][53] and guide the migration and followers follow the guide, connoting a subdivision of the group into distinct fractions [54]. Many mathematical models (stochastic models) have been developed to explain the various types of cell migration. However, these models are often based on the migration of clustered cells (tumors) or activated lymphocytes (taxis), whereas DPSCs, as said before, can migrate as single cells [55]. In addition, some models are based on the idea that the nucleus occupies a central position, but this is not always true. For example, in DPSCs, the nucleus is often lateral or in the back. Moreover, in response to environmental cues, many cells have the capacity to turn off their default migration mode from mesenchymal to ameboid and vice versa [56]. Another important feature to take into consideration is given by the stimuli that recruit the “leaders”, which is not fully understood and can be single or double. To date, the literature is still scarce concerning mathematical models that explain cell migration in the presence of two stimuli. The first cue concerns the choice of direction and the second, usually of mechanical origin, concerns the speed that the cell can reach going in that direction [57,58,59][57][58][59]. Speed is important because the fastest cells (leader) can lead the others (follower). However, further studies are needed to define a good mathematical model that accounts for the migration of DPSCs.

References

  1. Mitsiadis, T.A.; Catón, J.; Pagella, P.; Orsini, G.; Jimenez-Rojo, L. Monitoring Notch Signaling-Associated Activation of Stem Cell Niches within Injured Dental Pulp. Front. Physiol. 2017, 8, 372.
  2. Lizier, N.F.; Kerkis, A.; Gomes, C.M.; Hebling, J.; Oliveira, C.F.; Caplan, A.I.; Kerkis, I. Scaling-up of Dental Pulp Stem Cells Isolated from Multiple Niches. PLoS ONE 2012, 7, e39885.
  3. Xiao, X.; Xin, C.; Zhang, Y.; Yan, J.; Chen, Z.; Xu, H.; Liang, M.; Wu, B.; Fang, F.; Qiu, W. Characterization of Odontogenic Differentiation from Human Dental Pulp Stem Cells Using TMT-Based Proteomic Analysis. BioMed Res. Int. 2020, 2020, 3871496.
  4. Fujii, Y.; Kawase-Koga, Y.; Hojo, H.; Yano, F.; Sato, M.; Chung, U.-I.; Ohba, S.; Chikazu, D. Bone Regeneration by Human Dental Pulp Stem Cells Using a Helioxanthin Derivative and Cell-Sheet Technology. Stem Cell Res. Ther. 2018, 9, 24.
  5. Zhang, X.; Zhou, Y.; Li, H.; Wang, R.; Yang, D.; Li, B.; Cao, X.; Fu, J. Transplanted Dental Pulp Stem Cells Migrate to Injured Area and Express Neural Markers in a Rat Model of Cerebral Ischemia. Cell. Physiol. Biochem. 2018, 45, 258–266.
  6. Matsumura, H.; Marushima, A.; Ishikawa, H.; Toyomura, J.; Ohyama, A.; Watanabe, M.; Takaoka, S.; Bukawa, H.; Matsumura, A.; Matsumaru, Y.; et al. Induced Neural Cells from Human Dental Pulp Ameliorate Functional Recovery in a Murine Model of Cerebral Infarction. Stem Cell Rev. Rep. 2022, 18, 595–608.
  7. Driesen, R.B.; Hilkens, P.; Smisdom, N.; Vangansewinkel, T.; Dillen, Y.; Ratajczak, J.; Wolfs, E.; Gervois, P.; Ameloot, M.; Bronckaers, A.; et al. Dental Tissue and Stem Cells Revisited: New Insights From the Expression of Fibroblast Activation Protein-Alpha. Front. Cell Dev. Biol. 2020, 7, 389.
  8. Nito, C.; Sowa, K.; Nakajima, M.; Sakamoto, Y.; Suda, S.; Nishiyama, Y.; Nakamura-Takahashi, A.; Nitahara-Kasahara, Y.; Ueda, M.; Okada, T.; et al. Transplantation of Human Dental Pulp Stem Cells Ameliorates Brain Damage Following Acute Cerebral Ischemia. Biomed. Pharmacother. 2018, 108, 1005–1014.
  9. García-Sánchez, D.; Fernández, D.; Rodríguez-Rey, J.C.; Pérez-Campo, F.M. Enhancing Survival, Engraftment, and Osteogenic Potential of Mesenchymal Stem Cells. World J. Stem Cells 2019, 11, 748–763.
  10. Gronthos, S.; Mankani, M.; Brahim, J.; Robey, P.G.; Shi, S. Postnatal Human Dental Pulp Stem Cells (DPSCs) in Vitro and in Vivo. Proc. Natl. Acad. Sci. USA 2000, 97, 13625–13630.
  11. Al-Maswary, A.A.; O’Reilly, M.; Holmes, A.P.; Walmsley, A.D.; Cooper, P.R.; Scheven, B.A. Exploring the Neurogenic Differentiation of Human Dental Pulp Stem Cells. PLoS ONE 2022, 17, e0277134.
  12. Mousawi, F.; Peng, H.; Li, J.; Ponnambalam, S.; Roger, S.; Zhao, H.; Yang, X.; Jiang, L.H. Chemical Activation of the Piezo1 Channel Drives Mesenchymal Stem Cell Migration via Inducing ATP Release and Activation of P2 Receptor Purinergic Signaling. Stem Cells 2020, 38, 410–421.
  13. Du, Y.; Montoya, C.; Orrego, S.; Wei, X.; Ling, J.; Lelkes, P.I.; Yang, M. Topographic Cues of a Novel Bilayered Scaffold Modulate Dental Pulp Stem Cells Differentiation by Regulating YAP Signalling through Cytoskeleton Adjustments. Cell Prolif. 2019, 52, e12676.
  14. Matsunaga, M.; Kimura, M.; Ouchi, T.; Nakamura, T.; Ohyama, S.; Ando, M.; Nomura, S.; Azuma, T.; Ichinohe, T.; Shibukawa, Y. Mechanical Stimulation-Induced Calcium Signaling by Piezo1 Channel Activation in Human Odontoblast Reduces Dentin Mineralization. Front. Physiol. 2021, 12, 704518.
  15. Di Scipio, F.; Sprio, A.E.; Folino, A.; Carere, M.E.; Salamone, P.; Yang, Z.; Berrone, M.; Prat, M.; Losano, G.; Rastaldo, R.; et al. Injured Cardiomyocytes Promote Dental Pulp Mesenchymal Stem Cell Homing. Biochim. Biophys. Acta Gen. Subj. 2014, 1840, 2152–2161.
  16. Martens, W.; Wolfs, E.; Struys, T.; Politis, C.; Bronckaers, A.; Lambrichts, I. Expression Pattern of Basal Markers in Human Dental Pulp Stem Cells and Tissue. Cells Tissues Organs 2012, 196, 490–500.
  17. Li, K.; O’Dwyer, R.; Yang, F.; Cymerman, J.; Li, J.; Feldman, J.D.; Simon, M.; Rafailovich, M. Enhancement of Acellular Biomineralization, Dental Pulp Stem Cell Migration, and Differentiation by Hybrid Fibrin Gelatin Scaffolds. Dent. Mater. 2023, 39, 305–319.
  18. Küçükkaya Eren, S.; Bahador Zirh, E.; Zirh, S.; Sharafi, P.; Zeybek, N.D. Combined Effects of Bone Morphogenetic Protein-7 and Mineral Trioxide Aggregate on the Proliferation, Migration, and Differentiation of Human Dental Pulp Stem Cells. J. Appl. Oral Sci. 2022, 30, e20220086.
  19. Gronthos, S.; Arthur, A.; Bartold, P.M.; Shi, S. A Method to Isolate and Culture Expand Human Dental Pulp Stem Cells. In Mesenchymal Stem Cell Assays and Applications; Vemuri, M., Chase, L., Rao, M., Eds.; Humana Press: Totowa, NJ, USA, 2011; pp. 107–121. ISBN 978-1-60761-999-4.
  20. Patil, V.R.; Kharat, A.H.; Kulkarni, D.G.; Kheur, S.M.; Bhonde, R.R. Long Term Explant Culture for Harvesting Homogeneous Population of Human Dental Pulp Stem Cells. Cell Biol. Int. 2018, 42, 1602–1610.
  21. Lott, K.; Collier, P.; Ringor, M.; Howard, K.M.; Kingsley, K. Administration of Epidermal Growth Factor (EGF) and Basic Fibroblast Growth Factor (BFGF) to Induce Neural Differentiation of Dental Pulp Stem Cells (DPSC) Isolates. Biomedicines 2023, 11, 255.
  22. Xiao, N.; Yu, W.Y.; Liu, D. Glial Cell-Derived Neurotrophic Factor Promotes Dental Pulp Stem Cell Migration. J. Tissue Eng. Regen. Med. 2018, 12, 705–714.
  23. Bonnamain, V.; Thinard, R.; Sergent-Tanguy, S.; Huet, P.; Bienvenu, G.; Naveilhan, P.; Farges, J.C.; Alliot-Licht, B. Human Dental Pulp Stem Cells Cultured in Serum-Free Supplemented Medium. Front. Physiol. 2013, 4, 357.
  24. Hilkens, P.; Gervois, P.; Fanton, Y.; Vanormelingen, J.; Martens, W.; Struys, T.; Politis, C.; Lambrichts, I.; Bronckaers, A. Effect of Isolation Methodology on Stem Cell Properties and Multilineage Differentiation Potential of Human Dental Pulp Stem Cells. Cell Tissue Res. 2013, 353, 65–78.
  25. Kim, Y.; Park, J.-Y.; Park, H.-J.; Kim, M.-K.; Kim, Y.-I.; Kim, H.-J.; Bae, S.-K.; Bae, M.-K. Pentraxin-3 Modulates Osteogenic/Odontogenic Differentiation and Migration of Human Dental Pulp Stem Cells. Int. J. Mol. Sci. 2019, 20, 5778.
  26. Fatima, N.; Khan, A.A.; Vishwakarma, S.K. Immunophenotypic and Molecular Analysis of Human Dental Pulp Stem Cells Potential for Neurogenic Differentiation. Contemp. Clin. Dent. 2017, 8, 81–89.
  27. Huang, G.T.J.; Sonoyama, W.; Chen, J.; Park, S.H. In Vitro Characterization of Human Dental Pulp Cells: Various Isolation Methods and Culturing Environments. Cell Tissue Res. 2006, 324, 225–236.
  28. Senthilkumar, S.; Venugopal, C.; Parveen, S.; Shobha, K.; Rai, K.S.; Kutty, B.M.; Dhanushkodi, A. Remarkable Migration Propensity of Dental Pulp Stem Cells towards Neurodegenerative Milieu: An in Vitro Analysis. Neurotoxicology 2020, 81, 89–100.
  29. Lew, W.Z.; Feng, S.W.; Lin, C.T.; Huang, H.M. Use of 0.4-Tesla Static Magnetic Field to Promote Reparative Dentine Formation of Dental Pulp Stem Cells through Activation of P38 MAPK Signalling Pathway. Int. Endod. J. 2019, 52, 28–43.
  30. Alliot-Licht, B.; Hurtrel, D.; Gregoire, M. Characterization of A-Smooth Muscle Actin Positive Cells in Mineralized Human Dental Pulp Cultures. Arch. Oral Biol. 2001, 46, 221–228.
  31. Pagella, P.; Nombela-arrieta, C.; Mitsiadis, T.A. Distinct Expression Patterns of Cxcl12 in Mesenchymal Stem Cell Niches of Intact and Injured Rodent Teeth. Int. J. Mol. Sci. 2021, 22, 3024.
  32. Wei, X.-L.; Luo, L.; Chen, M.-Z.; Zhou, J.; Lan, B.-Y.; Ma, X.-M.; Chen, W.-X. Temporospatial Expression of Neuropeptide Substance P in Dental Pulp Stem Cells During Odontoblastic Differentiation In Vitro and Reparative Dentinogenesis In Vivo. J. Endod. 2023, 49, 276–285.
  33. Ehlinger, C.; Mathieu, E.; Rabineau, M.; Ball, V.; Lavalle, P.; Haikel, Y.; Vautier, D.; Kocgozlu, L. Insensitivity of Dental Pulp Stem Cells Migration to Substrate Stiffness. Biomaterials 2021, 275, 120969.
  34. Ganesh, V.; Seol, D.; Gomez-Contreras, P.C.; Keen, H.L.; Shin, K.; Martin, J.A. Exosome-Based Cell Homing and Angiogenic Differentiation for Dental Pulp Regeneration. Int. J. Mol. Sci. 2023, 24, 466.
  35. Rustom, A. The Missing Link: Does Tunnelling Nanotube-Based Supercellularity Provide a New Understanding of Chronic and Lifestyle Diseases? Open Biol. 2016, 6, 160057.
  36. Gao, Y.; Tian, Z.; Liu, Q.; Wang, T.; Ban, L.K.; Lee, H.H.C.; Umezawa, A.; Almansour, A.I.; Arumugam, N.; Kumar, R.S.; et al. Neuronal Cell Differentiation of Human Dental Pulp Stem Cells on Synthetic Polymeric Surfaces Coated with ECM Proteins. Front. Cell Dev. Biol. 2022, 10, 893241.
  37. Zhang, S.; Ye, D.; Ma, L.; Ren, Y.; Dirksen, R.T.; Liu, X. Purinergic Signaling Modulates Survival/Proliferation of Human Dental Pulp Stem Cells. J. Dent. Res. 2019, 98, 242–249.
  38. Miyazaki, A.; Sugimoto, A.; Yoshizaki, K.; Kawarabayashi, K.; Iwata, K.; Kurogoushi, R.; Kitamura, T.; Otsuka, K.; Hasegawa, T.; Akazawa, Y.; et al. Coordination of WNT Signaling and Ciliogenesis during Odontogenesis by Piezo Type Mechanosensitive Ion Channel Component 1. Sci. Rep. 2019, 9, 14762.
  39. Zheng, L.; Zhang, L.; Chen, L.; Jiang, J.; Zhou, X.; Wang, M.; Fan, Y. Static Magnetic Field Regulates Proliferation, Migration, Differentiation, and YAP/TAZ Activation of Human Dental Pulp Stem Cells. J. Tissue Eng. Regen. Med. 2018, 12, 2029–2040.
  40. Yang, J.-W.; Zhang, Y.-F.; Wan, C.-Y.; Sun, Z.-Y.; Nie, S.; Jian, S.-J.; Zhang, L.; Song, G.-T.; Chen, Z. Autophagy in SDF-1α-Mediated DPSC Migration and Pulp Regeneration. Biomaterials 2015, 44, 11–23.
  41. Du, L.; Feng, R.; Ge, S. PTH/SDF-1α Cotherapy Promotes Proliferation, Migration and Osteogenic Differentiation of Human Periodontal Ligament Stem Cells. Cell Prolif. 2016, 49, 599–608.
  42. Liang, C.; Liang, Q.; Xu, X.; Liu, X.; Gao, X.; Li, M.; Yang, J.; Xing, X.; Huang, H.; Tang, Q.; et al. Bone Morphogenetic Protein 7 Mediates Stem Cells Migration and Angiogenesis: Therapeutic Potential for Endogenous Pulp Regeneration. Int. J. Oral Sci. 2022, 14, 38.
  43. Li, J.; Diao, S.; Yang, H.; Cao, Y.; Du, J.; Yang, D. IGFBP5 Promotes Angiogenic and Neurogenic Differentiation Potential of Dental Pulp Stem Cells. Dev. Growth Differ. 2019, 61, 457–465.
  44. Vu, H.T.; Yoon, J.Y.; Park, J.H.; Lee, H.H.; Dashnyam, K.; Kim, H.W.; Lee, J.H.; Shin, J.S.; Kim, J. Bin The Potential Application of Human Gingival Fibroblast-Conditioned Media in Pulp Regeneration: An In Vitro Study. Cells 2022, 11, 3398.
  45. Zhou, C.; Duan, M.; Guo, D.; Du, X.; Zhang, D.; Xie, J. Microenvironmental Stiffness Mediates Cytoskeleton Re-Organization in Chondrocytes through Laminin-FAK Mechanotransduction. Int. J. Oral Sci. 2022, 14, 15.
  46. Li, B.; Liang, A.; Zhou, Y.; Huang, Y.; Liao, C.; Zhang, X.; Gong, Q. Hypoxia Preconditioned DPSC-Derived Exosomes Regulate Angiogenesis via Transferring LOXL2. Exp. Cell Res. 2023, 425, 113543.
  47. Wang, D.; Lyu, Y.; Yang, Y.; Zhang, S.; Chen, G.; Pan, J.; Tian, W. Schwann Cell-Derived EVs Facilitate Dental Pulp Regeneration through Endogenous Stem Cell Recruitment via SDF-1/CXCR4 Axis. Acta Biomater. 2022, 140, 610–624.
  48. Laudani, S.; La Cognata, V.; Iemmolo, R.; Bonaventura, G.; Villaggio, G.; Saccone, S.; Barcellona, M.L.; Cavallaro, S.; Sinatra, F. Effect of a Bone Marrow-Derived Extracellular Matrix on Cell Adhesion and Neural Induction of Dental Pulp Stem Cells. Front. Cell Dev. Biol. 2020, 8, 100.
  49. Hendijani, F. Explant Culture: An Advantageous Method for Isolation of Mesenchymal Stem Cells from Human Tissues. Cell Prolif. 2017, 50, e12334.
  50. Kok, Z.Y.; Alaidaroos, N.Y.A.; Alraies, A.; Colombo, J.S.; Davies, L.C.; Waddington, R.J.; Sloan, A.J.; Moseley, R. Dental Pulp Stem Cell Heterogeneity: Finding Superior Quality “Needles” in a Dental Pulpal “Haystack” for Regenerative Medicine-Based Applications. Stem Cells Int. 2022, 2022, 9127074.
  51. Marrelli, M.; Codispoti, B.; Shelton, R.M.; Scheven, B.A.; Cooper, P.R.; Tatullo, M.; Paduano, F. Dental Pulp Stem Cell Mechanoresponsiveness: Effects of Mechanical Stimuli on Dental Pulp Stem Cell Behavior. Front. Physiol. 2018, 9, 1685.
  52. Zhang, S.Y.; Ren, J.Y.; Yang, B. Priming Strategies for Controlling Stem Cell Fate: Applications and Challenges in Dental Tissue Regeneration. World J. Stem Cells 2021, 13, 1625–1646.
  53. Vishwakarma, M.; Thurakkal, B.; Spatz, J.P.; Das, T. Dynamic Heterogeneity Influences the Leader-Follower Dynamics during Epithelial Wound Closure: Heterogeneity Begets Better Coordination. Philos. Trans. R. Soc. B Biol. Sci. 2020, 375, 20190391.
  54. Müller, J.; Hense, B.A.; Fuchs, T.M.; Utz, M.; Pötzsche, C. Bet-Hedging in Stochastically Switching Environments. J. Theor. Biol. 2013, 336, 144–157.
  55. Qin, L.; Yang, D.; Yi, W.; Cao, H.; Xiao, G. Roles of Leader and Follower Cells in Collective Cell Migration. Mol. Biol. Cell 2021, 32, 1267–1272.
  56. Callan-Jones, A. Self-Organization in Amoeboid Motility. Front. Cell Dev. Biol. 2022, 10, 1000071.
  57. Loy, N.; Preziosi, L. Modelling Physical Limits of Migration by a Kinetic Model with Non-Local Sensing. J. Math. Biol. 2020, 80, 1759–1801.
  58. Loy, N.; Preziosi, L. Kinetic Models with Non-Local Sensing Determining Cell Polarization and Speed According to Independent Cues. J. Math. Biol. 2020, 80, 373–421.
  59. Conte, M.; Loy, N. Multi-Cue Kinetic Model with Non-Local Sensing for Cell Migration on a Fiber Network with Chemotaxis. Bull. Math. Biol. 2022, 84, 42.
More
© Text is available under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/)
ScholarVision Creations
Feedback